The role of vicariance and dispersal on the temporal range dynamics of forest vipers in the Neotropical region

Matheus Pontes-Nogueira; Marcio Martins; Laura R V Alencar; Ricardo J Sawaya

doi:10.1371/journal.pone.0257519

. 2021 Sep 17;16(9):e0257519. doi: 10.1371/journal.pone.0257519

The role of vicariance and dispersal on the temporal range dynamics of forest vipers in the Neotropical region

Matheus Pontes-Nogueira ^1,^¤,^*, Marcio Martins ², Laura R V Alencar ³, Ricardo J Sawaya ⁴

Editor: Tzen-Yuh Chiang⁵

PMCID: PMC8448354 PMID: 34534245

Abstract

The emergence of the diagonal of open/dry vegetations, including Chaco, Cerrado and Caatinga, is suggested to have acted as a dispersal barrier for terrestrial organisms by fragmenting a single large forest that existed in South America into the present Atlantic and Amazon forests. Here we tested the hypothesis that the expansion of the South American diagonal of open/dry landscapes acted as a vicariant process for forest lanceheads of the genus Bothrops, by analyzing the temporal range dynamics of those snakes. We estimated ancestral geographic ranges of the focal lancehead clade and its sister clade using a Bayesian dated phylogeny and the BioGeoBEARS package. We compared nine Maximum Likelihood models to infer ancestral range probabilities and their related biogeographic processes. The best fitting models (DECTS and DIVALIKETS) recovered the ancestor of our focal clade in the Amazon biogeographic region of northwestern South America. Vicariant processes in two different subclades resulted in disjunct geographic distributions in the Amazon and the Atlantic Forest. Dispersal processes must have occurred mostly within the Amazon and the Atlantic Forest and not between them. Our results suggest the fragmentation of a single ancient large forest into the Atlantic and Amazon forests acting as a driver of vicariant processes for the snake lineage studied, highlighting the importance of the diagonal of open/dry landscapes in shaping distribution patterns of terrestrial biota in South America.

Introduction

The Neotropical region is of great interest for the study of biogeographic processes. It has been shown to be the most biodiverse region in the world with high levels of endemism for different groups of organisms [1], including frogs [2], reptiles [3], and birds [4]. Several hypotheses have been proposed to explain this high diversity and endemism, including the Great American Biotic Interchange [5, 6], the isolation of South America as an island during the Paleogene and the Neogene (from 60 to 10 million years ago–mya; [7, 8]) and climatic fluctuations of the Pleistocene, from 2.6 mya to 12,000 years ago [9–12]. Such climatic fluctuations have been associated with the contraction and expansion of landscapes [11, 12].

The expansion of the South American diagonal of open/dry landscapes (DODL) including the Cerrado, Caatinga and Chaco ecoregions [13] (Fig 1), has raised the question of which processes have modulated the geographical distribution patterns of species we observe today in the Neotropical region. A recurring hypothesis in the literature is that the emergence of the DODL split a single large forest in South America prior to the Oligocene period into the present Atlantic and Amazon forests [10, 14–18] (Fig 1). Most of the formation of the DODL may have occurred due to two key factors: (i) the increasing aridity during cooler and drier periods that started in the Oligocene (between 28 and 25 mya; [13]); and (ii) the late Andean uplift throughout the late Miocene and early Pliocene (from 10 to 2 mya; Fig 1. [13, 19–21]), when the Andean Mountains reached its peak, between 6 to 4 mya [22]. The latter event has been suggested to have had a critical role on the last phases of the DODL formation, as the Andean uplift led to the uplift of the Brazilian Plateau and the subsidence of the Chaco region [13, 23]. Coscaron and Morrone [24] also hypothesized that the Andean uplift may have blocked the atmospheric flow from the Pacific Ocean, helping to increase aridity and the subsequent emergence of the DODL [24].

Whether the split acted as a vicariant process for terrestrial organisms [24, 30] or created a dispersal barrier preventing populations from one forest to reach the other has been debated [16, 31]. For assassin bugs of the Peiratinae subfamily and populations of the lizard species Polychrus marmoratus, it was hypothesized that the emergence of the DODL acted as a vicariant process [24, 30, 32]. For the frog genus Adenomera, numerous dispersals followed by vicariant events between the Amazon and DODL have been suggested, and one of these events have likely occurred between the Amazon and the Atlantic Forest, forming an Atlantic forest clade [28]. The DODL has also been suggested to have isolated the frogs of the genus Dendrophryniscus and Amazonella [33]. Lizards of the genus Enyalius colonized the Amazon from an Atlantic Forest ancestor in the late Oligocene, which corresponded to a cladogenetic event [27].

Historical connections between the two forest blocks through dispersal corridors within the DODL have been suggested (Fig 1) [10, 11, 34]. Such corridors, presently composed of relicts of the ancient large forest block, and including gallery forests of the Cerrado and the brejos of the Caatinga [10, 16], changed the view that the DODL is a separated and isolated region from both the Amazon and Atlantic forests [10]. Three major corridors have been proposed (see Fig 1) [10, 11, 26, 35]. The Eastern corridor would have connected the northern Atlantic Forest and eastern Amazon through the Caatinga region; the Central corridor would have been located in central Brazil, in the Cerrado region; and the Western corridor would have been located in southwestern South America, including the Chaco, in western Brazil, Paraguay, Bolivia, and Peru [10].

Those dispersal corridors in South America were apparently present during different geological periods (Fig 1) [34]. The Eastern and Central corridors possibly have opened up more recently, in the Quaternary [14, 15, 32, 34], during forest contractions and retractions in the Plio-Pleistocene epochs (~ last 5 mya; [9, 12, 36]). A recent study, however, suggests more ancient dispersal events through these “young pathways” in the early Miocene [27], 23 to 5 mya. The Western corridor, on the other hand, is hypothesized to be older and more relevant [34, 37], despite recent discussions about its importance [35]. The emergence of this corridor was congruent to sea introgressions forming the Pebas system, between 23 and 10 mya [21, 38, 39], with the expansion of the Amazon basin between 10 and 7 mya [21, 38], and with the emergence of the Paraná sea [40, 41]. Those events may have provided paths for terrestrial organisms to disperse [42]. Other studies have elaborated further on the Western corridor, suggesting that rather than a direct link between the Atlantic and Amazon forests, the corridor would have connected the Andean montane forests and the Southern Atlantic Forest [43–45]. At least two corridors may have connected the Andean region and the Atlantic Forest, one through the Chaco region, passing through Paraguay, northern Argentina and Bolivia, and the other within the Cerrado region, connecting the central Atlantic Forest and the Andes by gallery forests [45].

Snakes are an interesting model for understanding biogeographical processes. The group started to radiate more than 100 mya [46], and is distributed worldwide with the exception of Antarctica [47–50]. Thus, a myriad of processes might have shaped their current diversity and geographic patterns. Despite the great endemism and diversity of this group in the Neotropical region [51], it is only recently that the biogeographic processes responsible for this diversity have started to be studied [52–55]. Snakes of the family Viperidae, also known as vipers, are distributed worldwide and comprise approximately 360 species [56]. However, about 70% of all viper species are endemic to the New World [57].

The genus Bothrops in the viperid subfamily Crotalinae, commonly known as lanceheads, represents one of the most species-rich genus occurring in the New World [56] and, with the exception of few species, most of them are endemic to South America. Bothrops species are distributed in both forest blocks and open areas over the Neotropics, making them an ideal model for studying biogeographical processes in the Neotropical region. The group counts with recently phylogenies available [57, 58], and The Reptile Database [56] currently recognizes 45 species of lanceheads. Within these species, a group of 18 species stands out, as it is composed mainly by forest lanceheads, including Bothrops moojeni, which occurs in gallery forests throughout the Cerrado region [59], a geographic domain with savannah-like open vegetation.

Here we explored the hypothesis that the expansion of the DODL acted as a vicariant process for vipers of the genus Bothrops, by analyzing the temporal range dynamics of a Bothrops clade comprising 18 forest species, and using models of ancestral geographic range estimation. We intended to answer the following questions: (1) where did our focal forest clade originate?; and (2) how biogeographic processes such as vicariance and dispersal shaped the current geographic distribution of those species?

Materials and methods

Study area and regionalization

Different regionalization schemes have been proposed for the Neotropical Region [60–63]. Terrestrial ecoregions of the world represent a regionalization scheme based on global floristic maps and vegetation types [63, 64]. We used combinations of Neotropical ecoregions sensu Olson et al. [63] and Dinerstein et al. [64] to define our biogeographic units. Specifically, we defined 13 biogeographic units by combining ecoregions according to the distribution patterns of the focal clade (Fig 2).

Fig 2 — Biogeographical units are indicated by capital letters. Ecoregions or combinations of more than one ecoregion followed Olson et al. [63] and Dinerstein et al. [64] and were based on the present geographic range of *Bothrops* species. Images of *Bothrops* species are examples of some key species in each biogeographic unit. Photograph credits: Bruno Ferreto Fiorillo (*Bothrops jararacussu*), Marcio Martins (B. *moojeni*, B. *diporus* and B. *erythromelas*), Laurie J. Vitt (B. *taeniata* and B. *venezuelensis*), Conrado Mario da Rosa (B. *pubescens*), Herpetológica LAB from Mexico (B. *asper*), and Thibaud Aronson (B. *chloromelas*). Map source: Natural Earth (www.naturalearthdata.com).

Phylogenetic inference

To perform biogeographic analyses described below, we used the recently published molecular dataset provided by Carrasco et al. [58] to generate a dated molecular phylogeny for our focal clade. In their study, Carrasco et al. [58] generated a total evidence phylogeny of the genus Bothrops, with the description of a new species. Their dataset comprised only mitochondrial genes (12s, 16s, cox1, cytb and nd4), with 412 sequences. We used the R packages ape [65, 66] and seqinr [67] to retrieve the sequences from GenBank [68] using the accession numbers provided by Carrasco et al. [58]. We aligned the sequences with MAFFT version 7 online service [69–71] using default settings. The L-INS-I algorithm [72] was used to align genes 12s, 16s and cox1, and the FFT-NS-I algorithm [73] to align genes cytb and nd4. We used Gblocks 0.91b [74, 75] to remove poorly aligned positions of each sequence. We decided to allow gap positions within the final blocks in Gblocks. The sequences were then analysed and concatenated in MESQUITE 3.61 [76]. Our final sequence matrix contained 2,482 base pairs and 197 terminals. We used PartitionFinder 2.1.1 [77, 78] with a greedy algorithm and linked branch lengths to select the best partition scheme and corresponding substitution models for our gene matrix, partitioned by gene and codon position. The corrected Akaike Information Criterion (AICc) [79] was used to select the best fitted models (see S1 File for more info).

We estimated the phylogenetic relationships and divergence times using a Bayesian framework implemented in the software BEAST v2.6.4 [80, 81]. We estimated substitution rates using a relaxed uncorrelated lognormal clock [82]. We used a Birth-Death speciation model [83] as opposed to the Yule model [84], as the latter assumes zero extinction rates [85, 86] and it is commonly known that extinction has great importance in species diversification [87, 88]. We calibrated the phylogenetic relationships by using some of the age of divergence recovered by Alencar et al. [57] (see S1 File for more detail). Alencar et al. [57] generated a dated phylogeny comprising 79% of viper species using both mitochondrial and nuclear genes (six and five, respectively). These authors also dated their phylogeny using six fossils as calibration points, being two viperid fossils and four positioned in the outgroup. Although using fossils as calibration points is the best strategy to date phylogenies [89–92], the fossil record of vipers is scarce and only few fossils are considered suitable to be used as calibration points in phylogenetic analyses [57, 91, 92]. This is even more pronounced in Neotropical vipers, such as Bothrops. For this reason, we decided to date our phylogeny by using dates estimated by Alencar et al. [58], which were able to include several calibration points given their broader phylogenetic context. We decided to remove B. colombiensis and B. isabelae as they are not considered as separated species in recent taxonomic arrangements [56].

Geographic distribution data

Geographic distributions of each species were mostly based on the 4,158 raw point records obtained from Nogueira et al. [51]. For species not present in Nogueira et al. [51], we used the maps generated by Guedes et al. [93] and descriptions of the distributions provided by The Reptile Database [56]. The distribution of Bothrops sonene is available in Carrasco et al. [58]. Distributions can be seen in S2 File and S1 Fig. Species showing marginal geographic distributions in a biogeographic unit (< 10% of the total distribution records) were not considered as occurring in that unit (S2 File).

Ancestral geographic range estimation

Several models have been proposed to reconstruct ancestral geographic ranges [94], such as the Dispersal-Vicariance Analysis (DIVA; [95]), the Dispersal-Extinction-Cladogenesis (DEC; [96]), and the BayArea model [97]. DIVA is a parsimony model that considers vicariance more important than dispersal, giving different costs for this process (0 for vicariance, 1 for dispersal; [95]). Also, DIVA does not consider different processes that can occur among sympatric lineages (i.e. widespread and subset sympatry; [98]). DEC is a parametric model that implements two types of sympatric processes (narrow and subset; [98]). However, it lacks the implementation of widespread vicariance [98]. The BayArea is a Bayesian model that deals better with larger numbers of areas than other models, however it does not implement vicariant processes [98]. Recent implementations allow us to compare these models in a single platform, such as the package BioGeoBEARS in R software [98, 99]. BioGeoBEARS incorporates biogeographical models in a parametric and Maximum Likelihood (ML) environment. As the DIVA and BayArea are, respectively, parsimony and Bayesian models, they are implemented in BioGeoBEARS as DIVALIKE and BAYAREALIKE. These implementations are ML versions of the originals, with the biogeographic assumptions of such models, or processes that were originally implemented [98, 99], and not parsimony nor Bayesian approaches themselves. Details on how BioGeoBEARS interprets all biogeographical processes with examples from our results can be found in S1 Table.

We compared nine Maximum Likelihood (ML) models implemented in BioGeoBEARS, all of them representing variations of the three most used ML models: DEC, DIVALIKE, and BAYAREALIKE. Models can be set to estimate a certain maximum number of units in each ancestor, called the ‘maximum range size’. Changes in the maximum number of units can change the number of ranges possible in each node. The lower the maximum number of units, the lower the combinations possible. We set the maximum range size to 8, which is the number of units included in the range of Crotalus durissus. Note that C. durissus is a widespread Neotropical pit viper, showing the highest number of units within its geographical range, and for this reason we assumed that the ancestors had the potential to occur in up to 8 units. Although representing one of the major novelties of the BioGeoBEARS package [98–100], we did not include the parameter “j” (jump dispersal process) in our analyses due to recent discussions involving it [101]. Three models included a time stratified dispersal matrix (the "TS" models), that arbitrarily multiplies dispersal probabilities between two different regions based on landscape evolution of the Neotropical Region. Such probabilities range from 0 to 1, with 0 meaning that a geographic barrier prevents dispersal between two areas, and 1 meaning no dispersal limitations between two areas. Because we are testing the influence of the diagonal of open/dry landscapes, we decided to use the TS in our analysis. The explanation of how the time stratified matrix was created is available in S1 Text, and the S3 File contains the matrix itself. All models were compared using AIC [102], and the best fitting models were then analysed and discussed. As a supplementary analysis, we also performed the biogeographic reconstructions using the phylogeny generated by Alencar et al. [57] (S2 Fig).

Results

The topology recovered in the present study is similar to recent phylogenies generated for the group (S3 Fig) [57, 58]. More specifically, we also recovered Bothrops and Bothrocophias as paraphyletic due to the placement of B. lojanus within the latter. Within Bothrops, all major groups were recovered with high posterior probabilities, including the B. atrox (100%), B. jararacussu (100%), B. jararaca (100%), B. alternatus (96,64%) and B. neuwiedii groups (96,17%). After the removal of B. colombiensis and B. isabelae, our final phylogeny had 46 terminals.

We recovered the DECTS and DIVALIKETS models as best and second best model, respectively (Table 1). Both models included the time stratified matrix. DECTS was the best fitting model and had a better fit than the second-best evaluated model. However, the AIC difference between these two models was smaller than four, and the AIC weight of the second-best model was considerably high (0.24). Moreover, the DIVALIKETS was also recovered as the best fitted model when using the phylogeny generated by Alencar et al. [57] (S2 Fig). We therefore, consider to not have enough evidence to support one model over the other [103], and considered both models that estimated ancestral ranges under the phylogeny generated in this work to discuss the temporal range dynamics and evolutionary history of the group.

Table 1. Model comparisons on the ancestral range reconstruction of Bothrops forest clade performed with the phylogeny generated in this work.

d, e and w are free parameters in models where d is the rate of range expansion (i.e. dispersal), e is the rate of range contraction (i.e. extinction), and w is a dispersal multiplier parameter. As the time stratified matrix (TS models) were generated with arbitrary numbers, the “+w” models leave the w parameter free and the matrix itself is raised to the w parameter to seek the best dispersal multiplier values. Best models (DECTS and DIVALIKETS) are highlighted.

Models	Log likelihood	d	e	w	AIC	AIC weights
DECTS	-213.8	0.011	<0.0001	1	431.6	0.76
DIVALIKETS	-215	0.014	0.0054	1	433.9	0.24
DIVALIKETS+w	-220.7	0.01	<0.0001	0.014	447.4	0.0003
DEC	-221.8	0.0078	<0.0001	1	447.6	0.0003
DIVALIKE	-222.1	0.0095	0.002	1	448.1	0.0002
DECTS+w	-221.8	0.0078	<0.0001	0.0013	449.6	<0.0001
BAYAREALIKETS	-248.9	0.014	0.13	1	501.7	<0.0001
BAYAREALIKE	-252.5	0.011	0.14	1	508.9	<0.0001
BAYAREALIKETS+w	-252.3	0.011	0.14	0.037	510.7	<0.0001

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The most probable ancestral range reconstruction suggested the origin of the focal forest clade in the northwestern portion of South America (Node 1; unit D in DIVALIKETS and units ACD in DECTS, Fig 3 and S4 Fig, respectively). The Western Amazon biogeographical unit (D; see Fig 3) was recovered in both models in Node 1. However, geographical range probabilities reconstructed in DECTS are highly unresolved (S4 Fig), meaning that there are several other equally plausible combinations of biogeographical units that potentially represent the ancestral geographical range of the clade (this is why the pie chart is covered in black). Specifically, the range ACD has a probability of only 2.65% (S4 File) and is still the most probable ancestral range for this node, followed by ACDF (2.03%) and ABCDEF (1.90%). Under the DIVALIKETS model, on the other hand, ancestral range reconstruction is much more probable (Fig 4), as the range D has a probability of 33.33% (S4 File), followed by AD (17.85%) and DL (12,27%). The best-fitted model for Alencar et al.’s phylogeny [57] also recovered the Western Amazon as the most probable ancestral distribution of the forest focal clade (S2 Fig).

Fig 4 — Pie charts in nodes represent the geographic range probabilities of each hypothetical ancestor. Pie charts in the corners of the cladogram represent the geographical range probabilities inherited from the hypothetical ancestor immediately after a cladogenetic process. Colors represent biogeographical units. Units next to species names represent the current geographic distribution of each species. The green clade highlights the focal forest clade. Vertical dashed grey lines mark the time slices defined in the time stratified matrix. Focal nodes discussed in the text are numbered.

Vicariant processes occurred in nodes splitting lineages into two or more biogeographic units to its descendants (See Fig 3 and S4 Fig, and S1 Table for more details). In the Bothrops jararacussu group (Node 8), a vicariant process must have occurred splitting the lineages occurring in the Western Amazon (D) and the Southern Atlantic Forest (L) units (DL → L for the upper descendant, D for the lower descendant). Other vicariant processes must have taken place within the B. atrox group (Node 12). In Node 16, a vicariant event splitted lineages occurring in the Northern Amazon (F) and Northern Atlantic Forest (K) units (FK → K, F). Other vicariant processes in the forest clade explain diversification at nodes 5 (CD → D, C), 6 (AD → A, D), 14 (AF → A, F), and 17 (KL → L, K).

Dispersal processes (see S1 Table for details) between the Amazon and Atlantic forests may have primarily occurred: (i) before the ancestor of the B. jararacussu group emerged, between Node 7 upper descendant and Node 8 (D → DL); (ii) within the B. atrox group, between Node 15 lower descendant and Node 16 (F → FK); and in the lineage giving rise to B. bilineatus (D → DEFGK). Other dispersal events occurred in the lineage giving rise to B. moojeni, the only species inside the focal forest clade that reached the DODL, more specifically the Cerrado (L → IL).

Discussion

In this study, we investigated how the geographic ranges of a clade comprising 18 forest lanceheads changed across time, and which biogeographic processes were involved during the diversification of the clade in the Neotropical Region. The Western Amazon (D) biogeographic unit was the most probable ancestral geographic range of the clade, both for models selected using our phylogeny, based on the molecular dataset provided by Carrasco et al. [58] (Fig 3 and S4 Fig), and the best fitted model using Alencar et al.’s phylogeny [57] (S2 Fig). However, this result remains uncertain under the DECTS model (black pie charts in S4 Fig). Despite the DIVALIKETS being much more resolved, the Panama unit also appears at this node with high probability, representing the second most probable range distribution for the ancestor of the clade under DIVALIKETS. If a region comprising both Western Amazon and Panama units were the range of the clade’s ancestor, a vicariant process would have happened at the onset of the diversification of the clade. This vicariant event could have been potentially related to changes in the landscape that were occurring in those regions at the time, such as the uplift of the Andes [19–21] and the sea introgressions forming the Pebas system [21, 38, 104, 105]. Nevertheless, the most probable combinations of ancestral biogeographic units point to a northwestern South America origin for the forest clade, and most of these combinations include Amazonian units.

When focusing only on the groups that have a disjunct distribution on the forest blocks of the Neotropical Region, that is, those splitted by the DODL, a pattern of dispersal events followed by vicariance was detected, specifically vicariance events at nodes 8 and 16 and previous dispersal events. These events agree with the hypothesis of the expansion of the DODL in the Neotropical Region acting as a vicariant process, as already suggested for different groups of organisms [24, 30]. The formation of the diagonal was gradual and followed the late uplift of the Andes [14, 21], that reached its present height from 6 to 4 million years ago–mya [22]. This pattern of dispersal and vicariance is present in estimates under the DECTS (S4 Fig), DIVALIKETS (Figs 3 and 4) and under the best-fitted model (DIVALIKETS) using the phylogeny generated by Alencar et al. [57] (S2 Fig).

Fouquet et al. [28] found a similar pattern for the frog genus Adenomera, with a possible direct dispersal from the Amazon Forest to the Atlantic Forest followed by a vicariant process. According to those authors, the timeframe of this dispersal is concomitant with the ancient continuity between the two forest blocks [28]. It is probable that the formation of the DODL and subsequent split of the ancient forest connection led to the patterns observed. Other studies found dispersal processes between the two forest blocks followed by cladogenetic processes and lineage isolation. For the lizards of the genus Enyalius, the colonization of the Amazon from an Atlantic Forest ancestor occurred within the Oligocene (~ 25 mya) and led to further isolation of Enyalius leechii [27]. A similar pattern was observed for the lizards of the genus Anolis, although in the opposite direction, the colonization of the Atlantic Forest by an Amazonian ancestor [42].

Both vicariant processes found in our study (nodes 8 and 16) must have occurred in Plio-Pleistocene epochs (3–2 mya), which occurred more recently than those found by Fouquet et al. [28]. Some authors suggested much older vicariant events, between the Oligocene [27, 33] and early Miocene [28, 42]. Simon et al. [106] discuss that much of the Cerrado plant lineages began to diversify in the late Miocene (10 mya), and this late grassland expansion agrees with the even later vicariant events that we found here for the Bothrops clade. Coscarón and Morrone [24, 30], analysing members of the bug family Peiratinae, discuss that the disjunction patterns between the Atlantic and Amazon forests observed in many organisms occurred as a result of vicariant events, probably related to the expansion of the DODL influenced by the late Andean uplift in the Plio-Pleistocene, inducing aridity in South America through the interruption of the Pacific airflow [24, 107]. The late uplift of the Andes is also linked to the subsidence of the Chaco and the uplift of the Brazilian Plateau [13, 23]. Martins et al. [108] also found that the emergence of the DODL is congruent with a vicariant process in populations of the vampire bat Desmodus rotundus during the Pleistocene. A similar pattern of pleistocenic vicariance was suggested for birds from the genus Xiphorhynchus [109]. Forest expansions and contractions occurred at different times along the DODL [9, 12, 28, 106, 107], and this could explain the effect of the DODL in different timeframes. The results found here are congruent to these climatic and geological modifications in South America.

The only dispersal between the two forest blocks not followed by a vicariant event occured in the lineage giving rise to B. bilineatus. This species currently has a disjunct distribution in both the Atlantic and Amazon forests. Dal Vechio et al. [110] concluded in a phylogeographic approach that two different dispersal events probably occurred for this species, one at 2 mya ago, when the Atlantic Forest was colonized by a western Amazonian ancestor, and one more recently, at 0.3 mya, when an Atlantic Forest ancestor dispersed back to the Amazon Forest through the northeastern coast of Brazil [110]. The second dispersal event would be in line with the forest expansions and climatic fluctuations that occurred during the Quartenary [9, 11, 12], through the “young pathways” between the Atlantic and Amazon forests, as classified by Batalha-Filho et al. [34]. However, these pathways might have occurred much later [9, 11] and would correspond to the date of the second dispersal by B. bilineatus.

Perhaps more important than the vicariant processes themselves that occurred during the diversification of the clade of forest lanceheads is the almost lack of dispersal processes between the Amazon and the Atlantic forests. Dispersal events took place mostly: (i) within the Amazon units or between these Amazon units and the Caribbean and/or Andean units (B, C, D, E, F and G); and (ii) within the two Atlantic Forest units (K and L). Exceptions to this pattern are the three dispersals discussed above. This reinforces the DODL as a dispersal barrier between the two forest blocks, limiting the dispersal between them even after the Plio-Pleistocene climate fluctuations (2.5 mya) and forest expansions within the diagonal [9, 12, 16, 31]. Similar results are found for the frog genus Dendrophryniscus and Amazonella [33], Adenomera [28], and for the lizard genus Leposoma [29]. The restriction to forests and the lack of dispersion through open areas by forest lanceheads might suggest that niche conservatism could be prevalent in this clade. Indeed, the few dispersal events between the Amazon and Atlantic forests may even have happened through the forest corridors present within the DODL in the past, as highlighted for B. bilineatus [110]. Future studies could shed light on the usage of these corridors by other members of the Bothrops genus. Regardless of the pathways between the Amazon and the Atlantic forests within the DODL, our study indicates that the upper Miocene and Pliocene history of our clade was heavily influenced by the emergence of the DODL, as it may have acted both as a vicariant process in some lineages and as a dispersal barrier within our focal clade.

Conclusions

The ancestor of our focal clade of forest lanceheads was distributed in the northwestern Amazon forests, and the clade diversified over the Neotropical Region. Most of the dispersal events occurred within the Amazon and the Atlantic Forest, and not between them. Then, the DODL may have acted as a dispersal barrier between those forests. Moreover, the expansion of the diagonal is likely to have acted as a vicariant process for two clades of forest lanceheads.

Supporting information

S1 File. Beauti configurations.

The file consists of three sheets, the first showing the partitions used, the second the priors (without the calibration points) and the third the calibration points.

(XLSX)

Click here for additional data file.^{(14KB, xlsx)}

S2 File. Summary of the species distributions.

The file consists of two sheets. The first shows a summary of the distributions of all species, including source, range distribution, distributions not considered and reasons for not considering them. The source has a reference, and the number on its right side corresponds to the reference number present on References. The second sheet consists of the geographical file needed to run BioGeoBEARS. The numbers on the first line correspond to the number of species and biogeographical units used in this study, respectively. The letters correspond to the units. The 1s and 0s indicate the presence or absence of the species in an area, respectively. The order of the numbers corresponds to the order of the units in the first line.

(XLSX)

Click here for additional data file.^{(13KB, xlsx)}

S3 File. The time stratified matrix file.

It is divided into time slices corresponding to windows of millions of years. The values inside the matrix multiplies the dispersal probabilities between two areas (i.e. units), where 1 means no influence in the dispersal probability (total possibility of dispersal between two areas) and 0 means total influence in the dispersal probability (no possibility of dispersal between two areas). The values are all arbitrary. However, they are based on the known landscape evolution of the region covered by this study. Each line and column represent a unit. The units represented in the lines are the units from where the species dispersed, and in the columns are the units to which the species dispersed.

(TXT)

Click here for additional data file.^{(2.6KB, txt)}

S4 File. Percentages of every combination of units possible for every node in the forest lanceheads clade.

The nodes correspond to those present in the graphical results of both models (Figs 3 and 4 and S4 Fig). The file consists of two sheets, the first being for the DECTS model and the second being for the DIVALIKETS model.

(XLSX)

Click here for additional data file.^{(3MB, xlsx)}

S1 Fig. Distribution map of the species utilized in this study.

The occurrences indicated by squares are from Guedes et al. [93], and those dots are from Nogueira et al. [51]. The distributions that were recovered from Uetz et al. [56] and Carrasco et al. [58] are not shown, as they are descriptions. The units correspond to the units used in this study (Fig 2). Map made with Natural Earth. Free vector and raster map data from naturalearthdata.com.

(TIFF)

Click here for additional data file.^{(7.4MB, tiff)}

S2 Fig. Most probable ancestral range reconstructed by DIVALIKETS using Alencar et al.’ phylogeny.

Single capital letters indicate different biogeographical units used in this study. Mixed letters represent combinations of units. Colours also represent biogeographical units. Combinations of two or more units are shown as a mixed colour made from all the units in the combination. Units next to species names represent the current geographical distribution of each species. The green clade showcases the focal forest clade. Vertical dashed gray lines mark the time slices defined in the time stratified matrix. Letters in corners of the cladogram represent the geographical range inherited from the ancestor immediately after a cladogenetic process.

(TIFF)

Click here for additional data file.^{(781.6KB, TIFF)}

S3 Fig. Maximum credibility tree generated with Carrasco et al. [58] gene dataset used in this study.

Green clades were collapsed in the final phylogeny. Red clades were removed from the final phylogeny. Posterior probabilities higher than 0.75 are present at nodes (for some internal nodes we also occulted some posteriors for better visualization).

(TIFF)

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S4 Fig. Graphical results of DECTS.

(A) Ancestral geographic ranges reconstructed by the model. (B) Ancestral geographic range probabilities reconstructed by model. Nodes from the forest lanceheads clade are labelled. Single capital letters indicate different biogeographic units used in this study. Mixed letters represent combinations of units.Units next to species names represent the current geographic range of each species. The green clade showcases the focal forest clade. Vertical dashed grey lines mark the time slices defined in the time stratified matrix. Letters in corners of the cladogram represent the geographic range inherited from the ancestor immediately after a cladogenetic process.

(TIFF)

Click here for additional data file.^{(3MB, TIFF)}

S1 Table. Description of the processes considered by the models used in the work.

Examples are from the DIVALIKETS model. The table was heavily inspired and based on Matzke [98].

(DOCX)

Click here for additional data file.^{(40.7KB, docx)}

S1 Text. Explanation on how the time stratified matrix file was built.

(DOCX)

Click here for additional data file.^{(32.4KB, docx)}

Acknowledgments

We thank M. Carolina R. Manzano, Marcela Brasil Godinho, Leonardo M. Servino, Bruna Bolochio, and the Laboratório de Evolução e Diversidade 1 (LED1-UFABC) for insights and inspirations in earlier versions of the manuscript. We also thank Sam Hardman for English revision.

Data Availability

All relevant data are within the manuscript and its Supporting Information files.

Funding Statement

MPN was granted by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP; https://fapesp.br/) with the grant numbers Proc. 2014/23677-9 and Proc. 2017/11796-1. RJS was granted by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP; https://fapesp.br/) with the grant number proc. 2014/23677-9 and by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; https://www.gov.br/cnpq/pt-br) with the grant number 312795/2018-1. MM was granted by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP; https://fapesp.br/) with the grant number proc. 2018/14091-1 and by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; https://www.gov.br/cnpq/pt-br) with the grant number 306961/2015-6. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLoS One. doi: 10.1371/journal.pone.0257519.r001

Decision Letter 0

Tzen-Yuh Chiang

13 May 2021

PONE-D-21-11305

The role of vicariance and dispersal on the evolution of geographic distribution of forest vipers in the Neotropical region

PLOS ONE

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Reviewer #1: No

Reviewer #2: Yes

**********

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Reviewer #1: No

Reviewer #2: Yes

**********

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Reviewer #1: Yes

Reviewer #2: No

**********

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Reviewer #2: Yes

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Reviewer #1: Comments to authors:

Your manuscript entitled” The role of vicariance and dispersal on the evolution of geographic distribution of forest vipers in the Neotropical region" deals with an interesting topic. Unfortunately, however, I must reject your manuscript in the current version for the following reasons:

(1) I believe you need to reconstruct a new phylogenetic tree and divergence time tree comprising all species of the genus Bothrops. I suggest you generate a new dataset for all the five mtDNA genes which are common between Alencer et al.’s (2016) and Carrasco et al.’s (2019) studies. Alencer et al.’s dataset (2016) had numerous gaps and some species were partially covered for the 11 genes. For instance, Bothrops alcatraz was only covered for one gene (cyt b). For this reason, the divergence time tree is not reliable for BioGeoBEARS analysis, as it is sensitive to branch lengths.

(2) It appears that the results of your BioGeoBEARS analysis are not robust as you disregarded the four new species of the genus Bothrops.

Further Details regarding your BioGeoBEARS analysis:

- Line 164: What was the age of the root node? Was it included in the time slices?

- Line 164: What was the maximum range used for the BioGeoBEARS?

- Line 164: I would recommend considering the Area-adjacency, Area-allowed, and distance matrix in the analysis.

Reviewer #2: In this work, Pontes-Nogueira and collaborators address the macro-evolution of Bothrops pitvipers and their temporal range dynamics in South America, using for such purpose ancestral range reconstructions based on phylogenetic comparative models. Specifically, they test if the expansion of arid environments affected the evolution of this group. Despite the interest of the work, the current version of the ms requires to be improved for clarity in several aspects and along the distinct sections. Approaches and decisions have to be better explained and justified. The graphical part is quite limited and requires to be improved; and the discussion is a bit an extension of the results, without considering other terrestrial fauna that evolved in the region. Below I provide some comments to help the authors improve the ms.

Abstract

Line 19: terrestrial biodiversity rather than some lineages

Line 23: temporal range dynamics?

Lines 33-35: this conclusion is repetitive. Perhaps you can highlight how your work contribute to a better understanding of the biogeography and evolution of terrestrial biodiversity in South America.

Introduction

Lines 37 – 38: this first sentence is not well linked to the following information. Please consider to remove it, you can start with the second sentence in a very good way.

Line 46-48: do these vicariant processes result from the Pleistocene climatic oscillations (lines 44-46)? Pleistocene is a rather modern period and speciation events in reptiles (i.e. strictly referring to the formation of species) usually predate this time. Information from lines 45 to 48 must be set in the context of your work. In fact, in the next paragraph you explain the expansion of the DDL since the Oligocene and therefore, information in lines 45 to 48 seems out of context.

Line 49: Is it the expansion of the DDL or the existence/occurrence of these landscapes in between other?

Lines 49-104: isn’t any way to schematically represent these scenarios in a figure to improve the understanding of these processes and the location of barriers/corridors?

Line 64-65: I think it is better to refer to “terrestrial biodiversity” or something similar than “some lineages”

Lines 105-106: please, state why snakes are such interesting model.

Lines 111-113: please provide more information about this group of vipers. N of spp, ecology, habitat, ... etc.

Line 117: information about this forest clade should be clearly stated in the introduction. Is it constituted by the whole Bothrops? Or just by some lineages?

Line 118: please reinforce the biogeographical processes that you are thinking

Material & methods

Lines 125-126: why didn't you use the most recent work of these authors about biogeographical units?

Dinerstein, E., Olson, D., Joshi, A., Vynne, C., Burgess, N. D., Wikramanayake, E., ... & Saleem, M. (2017). An ecoregion-based approach to protecting half the terrestrial realm. BioScience, 67(6), 534-545.

Lines 142-146: the phylogeny of Bothrops with the supporting nodes could be presented in figure 1, with the map, specifying the major habitats for the clades (forest...).

Lines 151-155: this decision has to be better grounded. If the new phylogeny has more information that the one you are using but it is not dated, you can either (1) reconstruct a newer phylogeny for the group considering the information in both phylogenies and then date it; or (2) use the dating in Alencar et al to calibrate the new (and more complete) phylogeny.

Lines 158-159: a spatial representation of the distribution will help the reader to understand the following approach

Line 161: this explanation is vague. You could provide more info about what you consider "biological factors" here, in the main text.

Lines 165-184: I am missing some information about the models itself, what are their differences? Just provide a brief text for each one.

Lines 179-181: time stratified dispersal matrix could be provided in SM

Results

Is not there any way to graphically summarise range dynamics of Bothrops according to your results?

Lines 190-192: perhaps this information could be available in numeric format in SM

Lines 194-197: this interpretation of the results fits better in the discussion.

Line 242: please, explain how you reach this result. While ancestral ranges is easy to understand, I see complicated to follow your results for dispersal. This information is needed in M&M.

Lines 227-248: this text is quite difficult to follow because the figures have no numbers in the nodes

Discussion - it repeats the results and rarely goes far from the Bothrops group. Are not other groups that could support the discussion of your findings? In the introduction, several examples are provided to support the DDL. How do the studies developed in these fauna relate to your findings?

Line 251: first time using lanceheads!! If you use this term, this must be referred in the introduction.

Lines 262-263: please explain this better. What do you refer with “inclusive”?

Lines 308-310: which kind of recent studies? Please provide more information

Lines 314-315: please provide some examples of these future studies, will they target on genomics, landscape analysis, …?

Lines 315-318: this sentence fits much better in the conclusion

Conclusions

Briefly reinforce how by addressing the DDL hypothesis in Bothrops, your work does contribute to a better understanding of the biogeography and evolution of terrestrial biodiversity in South America.

Figure 1 – please consider to include the letters for each biogeographical unit (in the map) in the legend. Also, you could include the phylogeny, clearly signalling which the focal forest clade is.

**********

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Reviewer #2: No

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PLoS One. 2021 Sep 17;16(9):e0257519. doi: 10.1371/journal.pone.0257519.r002

Author response to Decision Letter 0

26 Jul 2021

We are very thankful for the comments and revisions on our manuscript made by the academic editor and the two reviewers of the initial text. Below is our response to every single point raised by both the editor and the reviewers to improve our work and to fully meet PLOS ONE’s publication criteria. We hope that we satisfyingly addressed these points and that our manuscript will now be suited for publication.

Sincerely,

On behalf of all authors,

Matheus Pontes-Nogueira (corresponding author).

Academic Editor

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Answer: We really appreciated this suggestion and opted to follow the second path. We remade all maps present in our work with public domain maps made available by Natural Earth. All map captions now have a disclaimer about the map construction, with a “Map source: Natural Earth (www.naturalearthdata.com).” at the end. We hope that now our images will not have any copyright implications.

Reviewer #1

Answer: we thank you immensely for this comment, as it was really helpful to fully improve our work. Both reviewers critiqued that we decided to not use the Carrasco et al. (2019) dataset, so we generated a new phylogeny using this dataset under a Bayesian framework. We then used calibration points accordingly with the dates estimated by Alencar et al. (2016) to date our phylogeny, as stated in the Material and Methods section of the new improved manuscript (lines 151 – 186, revised manuscript). However, we decided to not join both datasets and opted to run two separated analyses, one in the new phylogeny generated with the Carrasco et al.’s dataset and one with the phylogeny generated by Alencar et al. We then discuss the results in light of the results of both phylogenies, that are present both as figures in our manuscript and supplementary materials from our work. To help us with this work, we decided to include as an author Drª. Laura R. V. Alencar, the researcher responsible for the Alencar et al.’s phylogeny. We hope that this decision satisfyingly addresses this point raised by both reviewers.

(2) It appears that the results of your BioGeoBEARS analysis are not robust as you disregarded the four new species of the genus Bothrops.

Answer: Thanks for this advice. As stated before, we opted to construct a phylogeny using Carrasco et al.’s dataset, and we hope that now our analysis is robust with the inclusion of new species. However, it is worth noticing that the genetic dataset presented by Carrasco et al. do not include some of the species that these authors used to generate their phylogeny (that being B. sanctaecrusis, B. roedingeri, B. pirajai, B. otavioi and B. jonathani). This is due to lack of available genetic information of these species. Carrasco et al. generated a phylogeny using total evidence, and for these species they included morphological information that we can not use to generate a dated phylogeny with the methods used here. However, every specie that they did include a GenBank voucher we certainly used in our phylogenetic analysis.

Further Details regarding your BioGeoBEARS analysis:

- Line 164: What was the age of the root node? Was it included in the time slices?

Answer: the age of the root node was approximately 14 mya, as stated in our old supplementary material (titled S4 text in the old manuscript; line 25, fifth paragraph). As the age of the root node could be graphically seen in the results of the models, we decided to omit this information from the text. And indeed, it was included in the times slices (also stated in this supplementary material).

- Line 164: What was the maximum range used for the BioGeoBEARS?

Answer: previously it was set to 5. However it was set to 8 now due to the distribution of Crotalus durissus. We added a note in the Materials and Methods (lines 219 – 220) in the revised manuscript. Thanks for the suggestion.

- Line 164: I would recommend considering the Area-adjacency, Area-allowed, and distance matrix in the analysis.

Answer: Thanks for the suggestion. These models are very important, however our work is interest in the impact of the open/dry diagonal in the South America and, for this, we opted for not use these variations, as the time-stratified matrix already encompasses these landscape evolutions.

Reviewer #2

In this work, Pontes-Nogueira and collaborators address the macro-evolution of Bothrops pitvipers and their temporal range dynamics in South America, using for such purpose ancestral range reconstructions based on phylogenetic comparative models. Specifically, they test if the expansion of arid environments affected the evolution of this group. Despite the interest of the work, the current version of the ms requires to be improved for clarity in several aspects and along the distinct sections. Approaches and decisions have to be better explained and justified. The graphical part is quite limited and requires to be improved; and the discussion is a bit an extension of the results, without considering other terrestrial fauna that evolved in the region. Below I provide some comments to help the authors improve the ms.

Answer: We thank the reviewer for considering our manuscript of great interest. We are also very thankful for your considerations regarding our manuscript. We took into account almost all your considerations and indeed we all agree that our work is much more improved now. Specifically, we provide more details regarding our approaches and decisions, modified some aspects of our figures and included a new one (see Fig 1 in the new version of the manuscript). We also modified several aspects of the supplementary materials and made substantial changes in our results and discussion, providing more examples regarding the biogeography of other terrestrial organisms in the region. All of these aspects are detailed below in a our answers for each specific consideration.

Abstract

Line 19: terrestrial biodiversity rather than some lineages

Answer: Agreed! We changed this in the new revised manuscript. Thanks.

Line 23: temporal range dynamics?

Answer: We changed this in the new revised manuscript. We also changed our title to encompasses this suggestion. Thanks a lot.

Answer: we changed this in the revised manuscript, highlighting the importance of the open/dry diagonal in shaping distributions in South America. Thanks.

Introduction

Lines 37 – 38: this first sentence is not well linked to the following information. Please consider to remove it, you can start with the second sentence in a very good way.

Answer: Agreed! We removed this line in revised manuscript. Thanks.

Answer: Thanks for this comment. We reorganized this paragraph to make it better to understand and decided to remove the phrase that seems out of context.

Line 49: Is it the expansion of the DDL or the existence/occurrence of these landscapes in between other?

Answer: the expansion, that would be correlated with a vicariant processes accordingly with the hypothesis tested in the work!

Lines 49-104: isn’t any way to schematically represent these scenarios in a figure to improve the understanding of these processes and the location of barriers/corridors?

Answer: we are very thankful for this important comment, as it lead us to develop a figure that schematically represents all of these scenarios and times. The new figure (Fig 1 in the revised manuscript) graphically summarises all the landscape changes in South America regarding the expansion of the DODL. We believe that this image can help the reader to understand these changes in South America much more than the text (although the text is indispensable for explaining these changes as well). Once again we thank your for this suggestion.

Line 64-65: I think it is better to refer to “terrestrial biodiversity” or something similar than “some lineages”

Answer: Agreed! We changed this in revised manuscript. Thanks.

Lines 105-106: please, state why snakes are such interesting model.

Answer: we included a statement to why these organisms are so importante for biogeographic analysis (lines 108 – 111 in the revised manuscript). Thanks.

Lines 111-113: please provide more information about this group of vipers. N of spp, ecology, habitat, ... etc.

Answer: We provided much more information about this group in the revised manuscript (lines 116 – 125 in the revised manuscript). Thanks!

Line 117: information about this forest clade should be clearly stated in the introduction. Is it constituted by the whole Bothrops? Or just by some lineages?

Answer: We provided much more information about this specific clade (lines 122 – 125 in the revised manuscript). It is constituted by a clade of 18 species from the Bothrops genus. Thanks for this comment.

Line 118: please reinforce the biogeographical processes that you are thinking

Answer: Thanks. We reinforced the biogeographical processes (line 130).

Material & methods

Lines 125-126: why didn't you use the most recent work of these authors about biogeographical units?

Answer: Thanks for the suggestion. We were unaware about this recent work and considered it in our revised manuscript. However, it is worth noticing that almost nothing has changed for the Neotropical Region (i.e. the study region of the work) in this new work compared with the older work from Olson et al. So, we decided to cite both works in our regionalization scheme.

Lines 142-146: the phylogeny of Bothrops with the supporting nodes could be presented in figure 1, with the map, specifying the major habitats for the clades (forest...).

Answer: thanks for this suggestion, but we preferred to stay with the regionalization image that we presented in the old manuscript (with modifications, of course) and decided to include the phylogeny as a supplementary material, as the phylogenetic inference is not the focus of this work. Regarding the major habitats, the reconstruction results show the present distribution of the species utilized in this work right before the species names. Despite it, we decided to generate a image present in the supplementary material to help the reader in knowing the distribution of the species. See the next two comments. Thanks.

Answer: we REALLY appreciate this comment. Both reviewers critiqued that we decided to not use the Carrasco et al. (2019) dataset, so we generated a new phylogeny using this dataset under a Bayesian framework. We then used calibration points accordingly with the dates estimated by Alencar et al. (2016) to date our phylogeny, as stated in the Material and Methods section of the new improved manuscript (lines 151 – 186, revised manuscript). However, we decided to not join both datasets and opted to run two separated analyses, one in the new phylogeny generated with the Carrasco et al.’s dataset and one with the phylogeny generated by Alencar et al. We then discuss the results in light of the results of both phylogenies, that are present both as figures in our manuscript and supplementary materials from our work. To help us with this work, we decided to include as an author Drª. Laura R. V. Alencar, the researcher responsible for the Alencar et al.’s phylogeny. We hope that this decision satisfyingly addresses this point raised by both reviewers.

Lines 158-159: a spatial representation of the distribution will help the reader to understand the following approach

Answer: Thanks for the suggestion. We decided to make an image with all the distribution points of the species utilized in this work to help the reader in knowing the distributions of the species. The figure is present at the supplementary materials (S3 Fig). We really appreciated this comment.

Line 161: this explanation is vague. You could provide more info about what you consider "biological factors" here, in the main text.

Answer: we also deemed this statement confusing and decided to remove it from the manuscript. Thanks for the comment.

Lines 165-184: I am missing some information about the models itself, what are their differences? Just provide a brief text for each one.

Answer: information about the models were included in the revised manuscript for better understanding (lines 200 – 207). Thanks.

Lines 179-181: time stratified dispersal matrix could be provided in SM

Answer: we thank you for this suggestion, but the dispersal matrix was already present in the old manuscript. It was the S4 text and S3 file, and now they are the S5 text and S6 file respectively in the revised manuscript.

Results

Is not there any way to graphically summarise range dynamics of Bothrops according to your results?

Answer: thanks for the suggestion. We did not find a way to better represent these ranges dynamics besides the reconstructions per se. We elaborated further the results for better understanding and hope that it is now sufficient to understand the diversification within Bothrops.

Lines 190-192: perhaps this information could be available in numeric format in SM

Answer: thanks a lot for this suggestion. Percentages of all range combinations at every node inside our focal clade can now be seen at the S10 File in our supplementary material. We also elaborated further the results to include the percentages in the text. Thanks once again.

Lines 194-197: this interpretation of the results fits better in the discussion.

Answer: we agreed. We remove it from the Results. Thanks.

Line 242: please, explain how you reach this result. While ancestral ranges is easy to understand, I see complicated to follow your results for dispersal. This information is needed in M&M.

Answer: thanks for this comment. For better understanding of the process’s assumptions, we decided to create a table of processes considered in the BioGeoBEARS models. It can be seen at S4 Table in the supplementary materials of our work. We also elaborated further this paragraph for better understanding. We hope that now the assumptions about the processes will be clear to every reader.

Lines 227-248: this text is quite difficult to follow because the figures have no numbers in the nodes

Answer: Thanks for this comment. We included node numbers in our figure inside our focal clade for better understanding. Hope now it is easier to follow the results.

Discussion

it repeats the results and rarely goes far from the Bothrops group. Are not other groups that could support the discussion of your findings? In the introduction, several examples are provided to support the DDL. How do the studies developed in these fauna relate to your findings?

Answer: Thanks a lot for this comment. We elaborated further our discussion and revised the literature about this topic to compare our results with other researchers. Most of them where cited in the Introduction and now are discussed. We hope that now our discussion meets the expectations of the reviewers! Thanks once again.

Line 251: first time using lanceheads!! If you use this term, this must be referred in the introduction.

Answer: In the revised manuscript we decided to use this term since the beginning of the manuscript (Abstract, Introduction, etc.). Thanks for the suggestion.

Lines 262-263: please explain this better. What do you refer with “inclusive”?

Answer: we agreed that this sentence was confusing and decided to remove it in the revised manuscript. Thanks.

Lines 308-310: which kind of recent studies? Please provide more information

Answer: we provided much more information about the study that we cited in this line. We discuss and elaborate further this topics in lines 376 – 385 in the revised manuscript. Thanks for the suggestion.

Lines 314-315: please provide some examples of these future studies, will they target on genomics, landscape analysis, …?

Answer: future studies could target these forest corridors cited in the work and the use of these corridors by other members of the Bothrops genus. We elaborated it further in the Discussion (lines 399 – 403 in the revised manuscript).

Lines 315-318: this sentence fits much better in the conclusion

Answer: thanks for the suggestion, but as the conclusion already has a similar (but more focused) sentence, we decided to leave this sentence in the revised manuscript (lines 400 – 403).

Conclusions

Briefly reinforce how by addressing the DDL hypothesis in Bothrops, your work does contribute to a better understanding of the biogeography and evolution of terrestrial biodiversity in South America.

Answer: thanks for the suggestion. We tried to write a conclusion heavily focused in our results, as it already encompasses the importance of the DODL on the contribution to a better understanding of the biogeography in South America. For this, we made minor corrections in the Conclusion and decided to leave a similar conclusion in the revised manuscript (lines 406 – 411). We hope that the changes made in the discussion suggested by you support this conclusion. Thanks once again.

Figure 1

please consider to include the letters for each biogeographical unit (in the map) in the legend. Also, you could include the phylogeny, clearly signalling which the focal forest clade is.

Answer: we did include the letters for each biogeographical unit in the legend. Thanks for this suggestion. But, as stated before, we decided to not include the phylogeny in this Figure for a better visualization. The phylogeny can be seen in S8 Fig and the distribution of all species can be seen in S3 Fig. The focal forest clade can be clearly seen in both S8 Fig and Figs 3 and 4. Thanks once again.

Attachment

Submitted filename: Response to Reviewers.docx

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PLoS One. doi: 10.1371/journal.pone.0257519.r003

Decision Letter 1

Tzen-Yuh Chiang

16 Aug 2021

PONE-D-21-11305R1

The role of vicariance and dispersal on the temporal range dynamics of forest vipers in the Neotropical region

PLOS ONE

Dear Dr. Pontes-Nogueira,

Please submit your revised manuscript by Sep 30 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

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Tzen-Yuh Chiang

Academic Editor

PLOS ONE

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Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #2: Yes

**********

6. Review Comments to the Author

Reviewer #2: In this new version, Pontes-Nogueira and collaborators have successfully addressed most of my previous comments. There is a great improvement in the quality of the work in all methodological aspects, as well as in the way of transmitting the scientific reasoning, particularly in the introduction. The discussion has also been profoundly modified, now providing a good comparison of the results with the biogeography of different species in the region. My acknowledgements to the authors for such work!

I just have a few minor comments:

Line 155 - 159 – please add the number of sequences considered

Line 219-220 – please, explain better what you mean here and why you refer to Crotalus durissus

Lines 395-397 – you are not measuring or considering niche variables, so how your results could suggest anything about niche conservationism? Please, explain better.

Figs 3 and 4 – perhaps you could add a square or a lateral bar with the name of forest lanceheads after the names of the focal Bothrops to better highlight this group

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

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Reviewer #2: No

PLoS One. 2021 Sep 17;16(9):e0257519. doi: 10.1371/journal.pone.0257519.r004

Author response to Decision Letter 1

20 Aug 2021

Rebuttal Letter

We are very thankful for the comments and revisions on our revised manuscript made by the Academic editor and reviewer #2. Below is our response to every point raised by the editor and reviewer to improve our work and to fully meet PLOS ONE’s publication criteria. We hope that we satisfyingly addressed these points and that our manuscript will now be suited for publication.

Sincerely,

On behalf of all authors,

Matheus Pontes-Nogueira (corresponding author).

Academic Editor

Journal Requirements:

Answer: Thanks for this comment. We included 40 new citations in our manuscript in comparison to our original manuscript. However, we unfortunately forgot to mark in the ‘Revised Manuscript with Track Changes' these new references. This newer version has every new citation that we included in the revised manuscript marked accordingly. We further analysed all references to see if they meet PLOS ONE’s citation style and if they are corrected. We hope that now the reference list meets the journal’s criteria.

Reviewer #2

In this new version, Pontes-Nogueira and collaborators have successfully addressed most of my previous comments. There is a great improvement in the quality of the work in all methodological aspects, as well as in the way of transmitting the scientific reasoning, particularly in the introduction. The discussion has also been profoundly modified, now providing a good comparison of the results with the biogeography of different species in the region. My acknowledgements to the authors for such work! I just have a few minor comments:

Answer: We are very, very thankful for this comment. We are glad to know that we encompassed all the observations that you made in the revision. We hope that once again we fully addressed all your newer comments with this revised manuscript. Thanks once again!

Line 155 - 159 – please add the number of sequences considered

Answer: thanks for the comment. We added the number of sequences considered in the text (412 sequences; line 156). Thanks.

Line 219-220 – please, explain better what you mean here and why you refer to Crotalus durissus

Answer: We elaborated further this paragraph to explain better what the maximum range size is and why we used the range size of the C. durissus in our analysis (lines 219 – 225). We thank you for this advice and comment.

Lines 395-397 – you are not measuring or considering niche variables, so how your results could suggest anything about niche conservationism? Please, explain better.

Answer: we decided to expand this line to better explain how our results could suggest niche conservationism (lines 401-403). The lack of dispersal and the restriction to forest habitats could suggest that niche conservationism in this forest clade is important. We hope that now this statement is better explained. Thanks a lot for this comment.

Figs 3 and 4 – perhaps you could add a square or a lateral bar with the name of forest lanceheads after the names of the focal Bothrops to better highlight this group

Answer: thanks for the suggestion. We added a green square highlighting the names of the focal group. Thanks again.

Attachment

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Click here for additional data file.^{(19.1KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0257519.r005

Decision Letter 2

Tzen-Yuh Chiang

31 Aug 2021

PONE-D-21-11305R2

The role of vicariance and dispersal on the temporal range dynamics of forest vipers in the Neotropical region

PLOS ONE

Dear Dr. Pontes-Nogueira,

Please submit your revised manuscript by Oct 15 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

We look forward to receiving your revised manuscript.

Kind regards,

Tzen-Yuh Chiang

Academic Editor

PLOS ONE

Journal Requirements:

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #2: Yes

**********

6. Review Comments to the Author

Reviewer #2: In this new version, Pontes-Nogueira and collaborators have addressed all my comments. The manuscript looks fine, almost ready to be accepted for publication, except for few details in the added information about C. durissus which requires to be more specific and furthermore has a typo. Nevertheless, this is a very minor modification that can be easily solved.

Regarding this new information about C. durissus (lines 222-225):

First, the information in between () can be deleted because is repeating the information in the sentence, it does not provide any explanation. Second, I think that the authors must say something like “C. durissus is a widespread south American pit viper species showing the highest number of units within its range”. I guess, this is the reason why the authors look for other species out of the Bothrops clade to parameterise models. Finally, "specie" should be change by “species”.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: No

PLoS One. 2021 Sep 17;16(9):e0257519. doi: 10.1371/journal.pone.0257519.r006

Author response to Decision Letter 2

2 Sep 2021

Rebuttal Letter

We are very thankful for the comments and revisions on our revised manuscript made by the reviewer #2. Below is our response to every point raised by the reviewer to improve our work and to fully meet PLOS ONE’s publication criteria. We hope that we satisfyingly addressed these points and that our manuscript will now be suited for publication.

Sincerely,

On behalf of all authors,

Matheus Pontes-Nogueira (corresponding author).

Reviewer #2

In this new version, Pontes-Nogueira and collaborators have addressed all my comments. The manuscript looks fine, almost ready to be accepted for publication, except for few details in the added information about C. durissus which requires to be more specific and furthermore has a typo. Nevertheless, this is a very minor modification that can be easily solved.

Answer: thank you for these comments. We made the modifications that you suggested and hope that now the manuscript meets the journal standards. Thanks again.

Regarding this new information about C. durissus (lines 222-225):

Answer: We removed the information inside (). We also wrote something similar that you suggested (lines 219 – 226). Thanks for this suggestion because we see that it needed more information about C. durissus. And finally, there was no need for the change in “specie” because we rewrote the entire sentence. Thanks a lot for the suggestions.

Attachment

Submitted filename: Response to Reviewers.docx

Click here for additional data file.^{(17.8KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0257519.r007

Decision Letter 3

Tzen-Yuh Chiang

6 Sep 2021

The role of vicariance and dispersal on the temporal range dynamics of forest vipers in the Neotropical region

PONE-D-21-11305R3

Dear Dr.Pontes-Nogueira,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Tzen-Yuh Chiang

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #2: Yes

**********

6. Review Comments to the Author

Reviewer #2: (No Response)

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: No

PLoS One. doi: 10.1371/journal.pone.0257519.r008

Acceptance letter

Tzen-Yuh Chiang

9 Sep 2021

PONE-D-21-11305R3

The role of vicariance and dispersal on the temporal range dynamics of forest vipers in the Neotropical region

Dear Dr. Pontes-Nogueira:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Tzen-Yuh Chiang

Academic Editor

PLOS ONE

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 File. Beauti configurations.

The file consists of three sheets, the first showing the partitions used, the second the priors (without the calibration points) and the third the calibration points.

(XLSX)

Click here for additional data file.^{(14KB, xlsx)}

S2 File. Summary of the species distributions.

(XLSX)

Click here for additional data file.^{(13KB, xlsx)}

S3 File. The time stratified matrix file.

(TXT)

Click here for additional data file.^{(2.6KB, txt)}

S4 File. Percentages of every combination of units possible for every node in the forest lanceheads clade.

(XLSX)

Click here for additional data file.^{(3MB, xlsx)}

S1 Fig. Distribution map of the species utilized in this study.

(TIFF)

Click here for additional data file.^{(7.4MB, tiff)}

S2 Fig. Most probable ancestral range reconstructed by DIVALIKETS using Alencar et al.’ phylogeny.

(TIFF)

Click here for additional data file.^{(781.6KB, TIFF)}

S3 Fig. Maximum credibility tree generated with Carrasco et al. [58] gene dataset used in this study.

(TIFF)

Click here for additional data file.^{(765.6KB, TIFF)}

S4 Fig. Graphical results of DECTS.

(TIFF)

Click here for additional data file.^{(3MB, TIFF)}

S1 Table. Description of the processes considered by the models used in the work.

Examples are from the DIVALIKETS model. The table was heavily inspired and based on Matzke [98].

(DOCX)

Click here for additional data file.^{(40.7KB, docx)}

S1 Text. Explanation on how the time stratified matrix file was built.

(DOCX)

Click here for additional data file.^{(32.4KB, docx)}

Attachment

Submitted filename: Response to Reviewers.docx

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Click here for additional data file.^{(19.1KB, docx)}

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Submitted filename: Response to Reviewers.docx

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Data Availability Statement

All relevant data are within the manuscript and its Supporting Information files.

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The role of vicariance and dispersal on the temporal range dynamics of forest vipers in the Neotropical region

Matheus Pontes-Nogueira

Marcio Martins

Laura R V Alencar

Ricardo J Sawaya

Roles

Abstract

Introduction

Fig 1. Summary of important events underlying the expansion of the diagonal of open/dry landscapes (DODL).

Materials and methods

Study area and regionalization

Fig 2. Regionalization scheme used in this study.

Phylogenetic inference

Geographic distribution data

Ancestral geographic range estimation

Results

Table 1. Model comparisons on the ancestral range reconstruction of Bothrops forest clade performed with the phylogeny generated in this work.

Fig 3. Ancestral geographic ranges of the Bothrops forest clade reconstructed under the DIVALIKETS model.

Fig 4. Ancestral geographic range probabilities associated with the range reconstruction of Bothrops forest clade under the DIVALIKETS model.

Discussion

Conclusions

Supporting information

Acknowledgments

Data Availability

Funding Statement

References

Decision Letter 0

Tzen-Yuh Chiang

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Author response to Decision Letter 0

Decision Letter 1

Tzen-Yuh Chiang

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Author response to Decision Letter 1

Decision Letter 2

Tzen-Yuh Chiang

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Author response to Decision Letter 2

Decision Letter 3

Tzen-Yuh Chiang

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Acceptance letter

Tzen-Yuh Chiang

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Associated Data

Supplementary Materials

Data Availability Statement

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