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. 2020 Nov 13;9(11):1569. doi: 10.3390/plants9111569

Biogeography of Stigmaphyllon (Malpighiaceae) and a Meta-Analysis of Vascular Plant Lineages Diversified in the Brazilian Atlantic Rainforests Point to the Late Eocene Origins of This Megadiverse Biome

Rafael Felipe de Almeida 1,2,*, Cássio van den Berg 1
PMCID: PMC7696469  PMID: 33203045

Abstract

We investigated the biogeography of Stigmaphyllon, the second-largest lianescent genus of Malpighiaceae, as a model genus to reconstruct the age and biogeographic history of the Brazilian Atlantic Rainforest (BAF). Few studies to date have focused on the tertiary diversification of plant lineages in the BAFs, especially on Stigmaphyllon. Phylogenetic relationships for 24 species of Stigmaphyllon (18 ssp. From the Atlantic forest (out of 31 spp.), three spp. from the Amazon Rainforest, two spp. from the Caatinga biome, and a single species from the Cerrado biome) were inferred based on one nuclear DNA (PHYC) and two ribosomal DNA (ETS, ITS) regions using parsimony and Bayesian methods. A time-calibrated phylogenetic tree for ancestral area reconstructions was additionally generated, coupled with a meta-analysis of vascular plant lineages diversified in the BAFs. Our results show that: (1) Stigmaphyllon is monophyletic, but its subgenera are paraphyletic; (2) the most recent common ancestor of Stigmaphyllon originated in the Brazilian Atlantic Rainforest/Caatinga region in Northeastern Brazil ca. 26.0 Mya; (3) the genus colonized the Amazon Rainforest at two different times (ca. 22.0 and 6.0 Mya), the Caatinga biome at least four other times (ca. 14.0, 9.0, 7.0, and 1.0 Mya), the Cerrado biome a single time (ca. 15.0 Mya), and the Southern Atlantic Rainforests five times (from 26.0 to 9.0 Mya); (4) a history of at least seven expansion events connecting the Brazilian Atlantic Rainforest to other biomes from 26.0 to 9.0 Mya, and (5) a single dispersion event from South America to Southeastern Asia and Oceania at 22.0 Mya via Antarctica was proposed. Compared to a meta-analysis of time-calibrated phylogenies for 64 lineages of vascular plants diversified in the Brazilian Atlantic Rainforests, our results point to a late Eocene origin for this megadiverse biome.

Keywords: ancestral area reconstruction, Atlantic rainforest, time-calibrated phylogenies, Malpighiales, neotropical flora

1. Introduction

Malpighiaceae Juss. is one of the most diverse plant families of Neotropical shrubs, trees, and lianas [1], with most species confined to this region [2]. Its species are easily recognized by their remarkable floral conservatism, with flowers frequently bearing a pair of oil-secreting glands at the base of sepals, petals clawed at the base, and a posterior petal differentiated from the remaining lateral four [1,2]. This family has received broad phylogenetic attention in the past few years [2,3,4,5,6,7,8], including more focused investigations on generic delimitations and the phylogenetic position of Old-World clades [2,6]. However, there have been few efforts to determine finer-scale patterns of molecular analyses and historical biogeography in Neotropical Malpighiaceae [4,6,8,9].

Stigmaphyllon A.Juss. is one of the several genera in Malpighiaceae re-circumscribed due to recent molecular phylogenetic studies [2,6]. It is currently the second-largest lianescent genus in Malpighiaceae and the only occurring in forested habitats in the tropics and subtropics of America, Africa, Asia, and Oceania [10]. Most species are woody lianas with long-petioled, elliptical to cordate leaves, corymbs or umbels of yellow flowers arranged in dichasia, styles holding laterally expanded appendages in the apex, and schizocarpic fruits splitting into three-winged mericarps, bearing a sizeable dorsal wing (Figure 1 a–h) [10,11]. This genus is currently divided into two subgenera, Stigmaphyllon and Ryssopterys, treated as separate genera before molecular phylogenies [10]. Stigmaphyllon subgenus Stigmaphyllon includes ca. 90 species restricted to the Neotropics, except for Stigmaphyllon bannisterioides A.Juss., which is also found in West Africa [11]. On the other hand, S. subgenus Ryssopterys includes ca. 20 species restricted to Southeast Asia and Oceania [10]. The monophyly of Stigmaphyllon and its subgenera has been suggested by previous phylogenetic studies but never adequately corroborated because its type species was never sampled [2,3,5,6].

Figure 1.

Figure 1

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Phylogram from the combined analysis of nuclear and ribosomal markers for Stigmaphyllon. Posterior probabilities are shown above branches and bootstrap values below branches. Black bars represent S. subg. Stigmaphyllon and the white bar represents S. subg. Ryssopterys. (dark blue bar) S. paralias group; (yellow bar) S. ciliatum group; (dark green bar) S. subg. Ryssopterys; (orange bar) S. finlayanum group; (purple bar) S. auriculatum group; (light green bar) S. urenifolium group; (light blue bar) S. lalandianum group; (red bar) S. sinuatum group; (pink bar) S. blanchetii group; (grey bar) S. saxicola group. (A) adaxial surface of a leaf of S. angustilobum A.Juss. (B) Umbel of S. ciliatum (Lam.) A.Juss. in side view evidencing ciliate reduced leaves associated with the inflorescence. (C) open flower of S. ciliatum in frontal view. (D) androecium and gynoecium of S. ciliatum in side view, (E) mericarp of S. paralias A.Juss. in side view. (F) winged mericarp of S. ciliatum in side view. (G) winged mericarp of S. auriculatum (Cav.) A.Juss. in side view. (H) winged mericarp of S. saxicola C.E.Anderson in side view. (I) winged mericarps of S. blanchetii in side view (photographs by R.F.Almeida).

Previous phylogenetic studies for Malpighiaceae suggested a Brazilian Atlantic Rainforest (herein treated as BAF) origin for Stigmaphyllon, with S. paralias A.Juss. being consistently recovered in several studies as the first lineage to diverge in the genus [2,6]. Even though the BAFs currently comprise more than 15,000 known vascular plant species [12], they are regarded as one of the most threatened hotspots for biodiversity worldwide due to being mostly fragmented and disturbed by most of Brazil’s human population and economic activity [13]. Several biogeographic hypotheses have been proposed to explain the origins of the great biodiversity of the BAFs, such as: 1. Miocene to Pleistocene forest corridors between BAFs and the Amazon rainforests via Cerrado’s gallery forests and/or via the coastal region in Northeastern Brazil [14]; and 2. Pleistocene refugia hypothesis, which suggested that Pleistocene climatic fluctuations led to rainforest fragmentation and promoted divergence of lineages or species in isolated forest fragments or refugia [15]. Pleistocene diversifications in BAFs have been greatly criticized due to the lack of concordance with empirical phylogenetic data, as well as by the evidence that shifts in forest species distribution, rather than fragmentation, have been the main consequences of global glaciations in the Neotropics [16]. Although most previous studies have focused on explaining BAFs biodiversity through Miocene to Pleistocene climatic/geological events, no study to date has focused on timing the age of vascular plant lineages diversification in BAFs.

In this study, we focus on timing the biogeographic history of BAFs using Stigmaphyllon as a model genus, supplemented by a meta-analysis of vascular plant lineages diversified in this biome to infer the age of BAFs. More specifically, we: (1) test the monophyly of Stigmaphyllon and its subgenera; (2) time-calibrate the phylogenetic tree; (3) estimate the ancestral areas of Stigmaphyllon; and (4) shed some light on the age and biogeographic history of BAFs using Stigmaphyllon and a meta-analysis of vascular plant lineages diversified in this biome.

2. Results

2.1. Phylogenetic Analysis

Our combined dataset for ribosomal (ETS, ITS) and nuclear (PHYC) markers contains a total of 2283 characters, of which 1724 characters are constant, 257 characters are variable, but parsimony uninformative, and 302 characters are parsimony informative. The combined analysis of nuclear and ribosomal markers provides higher support for more clades than those based on independent nuclear and ribosomal datasets. Overlapping peaks (paralogous copies) for ETS and ITS were not recorded during electrophoresis and sequencing. The heuristic search for the combined dataset found 15 trees (consistency index, CI = 0.80, retention index, RI = 0.70), and the strict consensus tree includes 17 moderately supported clades (bootstrap percentage, BP > 75; Figure 1). The Bayesian analysis recovered 25 well-supported to moderately supported clades (posterior probabilities, PP > 0.95 and >0.80, respectively; Figure 1).

The monophyly of Stigmaphyllon (Figure 1) is strongly supported by Maximum Parsimony (MP) and Bayesian Inference (BI) analyses, being recovered as sister to Diplopterys. The clade Stigmaphyllon + Diplopterys is well supported (BS100/PP1.0) as sister to Bronwenia (Figure 1). Within Stigmaphyllon, Stigmaphyllon subg. Stigmaphyllon is recovered as polyphyletic, with its representatives placed in three separate lineages (Figure 1, black bars), named: the early-diverging Stigmaphyllon paralias group (Figure 1, dark blue bar), Stigmaphyllon ciliatum group (Figure 1, yellow bar) and core Stigmaphyllon (here represented by the common ancestor that the lineage S. fynlayanum + S. puberulum share with the remaining species (Figure 1, black bar)). Stigmaphyllon subg. Ryssopterys (Figure 1, dark green bar) is recovered as monophyletic in our analyses, being sister to the Stigmaphyllon ciliatum group (Figure 1, white bar).

Within core Stigmaphyllon, seven major lineages are recovered, here designated as 1. S. puberulum group, 2. S. auriculatum group, 3. S. urenifolium group, 4. S. lalandianum group, 5. S. sinuatum group, 6. S. blanchetii group, and 7. S. gayanum group. The S. puberulum group (Figure 1, orange bar) is well-supported (BS100/PP1.0), comprising only two species, S. finlayanum A.Juss. and S. puberulum Griseb., while the S. auriculatum group (Figure 1, purple bar) is moderate to well-supported (B77/PP1.0), comprising three species, S. angustilobum A.Juss., S. arenicola C.E.Anderson, and S. auriculatum (Cav.) A.Juss. The S. urenifolium group (Figure 1, light green bar) is weak to well-supported (BS70/PP1.0), represented by only its naming species. In contrast, the S. lalandianum group (Figure 1, light blue bar) is moderate to well-supported (BS82/PP1.0), comprising four species, S. alternifolium A.Juss., S. bonariense (Hook. and Arn.) C.E.Anderson, S. lalandianum A.Juss., and S. vitifolium A.Juss. The S. sinuatum group (Figure 1, red bar) is well-supported (BS100/PP1.0), represented by only two species, S. lindenianum A.Juss. and S. sinuatum (DC.) A.Juss., while the S. blanchetii group (Figure 1, rose bar) is weakly-supported (BS-/PP0.60), comprising four species, S. blanchetii C.E.Anderson, S. caatingicola R.F.Almeida and Amorim, S. jatrophifolium A.Juss., and S. salzmannii A.Juss. Finally, the S. gayanum group (Figure 1, gray bar) is weakly to well-supported (BS-/PP1.0), and represented by four species, S. cavernulosum C.E.Anderson, S. gayanum A.Juss., S. macropodum A.Juss., and S. saxicola C.E.Anderson.

2.2. Ancestral Area Reconstruction and Divergence Times Estimation

The S-DEC reconstruction suggests that the most recent common ancestor (MRCA) of Stigmaphyllon was widespread in the northern portion of the BAFs ca. 26.0 Mya (Figure 2 and Figure 3, node 3, Table 1). A dispersal event (node 3) took place then, splitting the MRCA of the Stigmaphyllon paralias group from the remaining species, which dispersed from Seasonally Dry Tropical Forests (SDTFs) to Campos Rupestres in northeastern Brazil ca. 14.0 Mya (Figure 2 and Figure 3, node 4, Table 1). The MRCA of the S. ciliatum and S. timoriense (DC.) C.E.Anderson clade diverged ca. 22.0 Mya (node 5) and split into those lineages ca. 10.0 Mya (node 6), colonizing dunes vegetation on the Atlantic and Australasian rainforests (Figure 2 and Figure 3, node 6, Table 1). The MRCA of core Stigmaphyllon dispersed to the southern portion of the BAFs ca. 19.0 Mya (Figure 2 and Figure 3, node 7, Table 1). The MRCA of the S. puberulum group arose 6.25 Mya, being widespread over both the Amazon and Atlantic rainforests, with a vicariant event giving rise to its current lineages (Figure 2 and Figure 3, node 8, Table 1). The MRCA of the remaining species (node 9) remained distributed in the BAFs ca. 17.0 Mya, giving rise to the MRCA of the S. auriculatum group ca. 9.4 Mya (node 10). A dispersal event followed by the colonization of dunes vegetation in Southern Brazil gave rise to the S. arenicola lineage (Figure 2 and Figure 3, node 10, Table 1). In the Pleistocene, ca. 0.72 Mya, the MRCA of the S. auriculatum and S. angustilobum arose in the BAFs from Southeastern Brazil, giving rise to those lineages via a dispersal event from rainforests to SDTFs (Figure 2 and Figure 3, node 11, Table 1). The MRCA of S. urenifolium (Figure 2 and Figure 3, node 12, Table 1) arose ca. 15.0 Mya via a dispersal and a vicariant event from the BAFs to the Cerrado. The MRCA of the remaining species (Figure 2 and Figure 3, node 13, Table 1) arose ca. 13.0 Mya in the BAFs and, probably, in the Amazon forest, as well. The MRCA of node 14 remained distributed within the Southeastern portion of the BAFs ca. 7.0 Mya (Figure 2 and Figure 3, node 14, Table 1) and diversified into its four main lineages ca. 4.0 Mya (Figure 2 and Figure 3, nodes 15–16, Table 1). Both a dispersal and a vicariant event took place ca. 12.0 Mya giving rise to the MRCA of node 17, which was distributed within the BAFs, Caatinga, and the Amazon rainforest. The lineage of node 18 colonized the Amazon rainforest for the first time, but only diversified ca. 0.5 Mya (Figure 2 and Figure 3, node 18, Table 1).

Figure 2.

Figure 2

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Chronogram and Statistical-Dispersal-Extinction-Cladogenesis (S-DEC) ancestral area reconstructions for Stigmaphyllon. Nodes are numbered from 1 to 26. Numbers above branches represent estimated ages (Mya). Branch letters on the left represent the reconstructed ancestral area(s): (A) Atlantic rainforest; (B) Seasonally Dry Tropical Forest; (C) Amazon rainforest; (D) Cerrado; (E) Australasian rainforests. Branch letters on the right represent dispersal (d) or vicariant (v) events.

Figure 3.

Figure 3

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Times of dispersal/vicariance events leading to biome shifting in Stigmaphyllon. (blue) Atlantic rainforest; (purple) Seasonally Dry Tropical Forest; (orange) Amazon Rainforest; (red) Cerrado. Green circles represent the original ancestral populations of Stigmaphyllon. Dark circles represent populations of Stigmaphyllon colonizing new biomes over different time periods.

Table 1.

Divergence times estimates (maximum/mean/minimum), ancestral area reconstructions, and dispersal/vicariance events reconstructed for all nodes in this study.

Nodes Max Age
Mean		 Min Ancestral Area Reconstruction Dispersal/Vicariance Event
1 40.0 39.95 35.0 Atlantic Forest/Caatinga Dispersal
2 41.29 36.39 29.92 Atlantic Forest/Caatinga Dispersal
3 34.09 26.47 19.35 Atlantic Forest Dispersal
4 22.14 14.06 6.76 Caatinga Dispersal
5 30.14 22.41 15.43 Atlantic Forest Dispersal
6 19.87 10.18 2.18 Atlantic Forest/Asian Rainforests Vicariance
7 26.14 19.19 12.71 Atlantic Forest Dispersal
8 12.35 6.25 1.06 Atlantic Forest/Caatinga/Amazon Forest Vicariance
9 24.05 17.45 11.64 Atlantic Forest -
10 16.22 9.4 3.18 Atlantic Forest Dispersal
11 1.81 0.72 0.03 Atlantic Forest/Caatinga Dispersal
12 21.40 15.21 10.06 Atlantic Forest Dispersal/Vicariance
13 18.30 12.89 8.25 Atlantic Forest -
14 12.16 7.45 3.30 Atlantic Forest -
15 8.70 4.57 1.42 Atlantic Forest -
16 8.29 4.39 0.95 Atlantic Forest -
17 17.19 12.01 7.32 Atlantic Forest Dispersal/Vicariance
18 1.84 0.54 0.0 Amazon Forest -
19 16.0 11.09 6.88 Atlantic Forest Dispersal
20 13.05 8.52 4.43 Atlantic Forest -
21 10.87 6.73 3.04 Atlantic Forest Dispersal
22 8.49 4.81 1.28 Atlantic Forest -
23 13.49 8.98 4.88 Atlantic Forest/Caatinga Dispersal
24 0.36 0.30 0.10 Caatinga -
25 10.35 6.06 2.27 Atlantic Forest/Caatinga Dispersal
26 0.86 0.27 0.0 Atlantic Forest/Caatinga Dispersal
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2.3. Meta-Analysis

We identified 113 genera of ferns/lycophytes, gymnosperms, magnoliids, monocots, and eudicots comprising lineages exclusively diversified in the BAF biome (out of a total of 2224 genera currently recorded by the Flora do Brasil Project; Table 2). Only 64 of those genera have estimated diversification ages available from 34 phylogenetic studies published from 2004 to 2020 (Figure 4, Table 2). Most of those studies were published from 2015 to 2020 when molecular clocks and time-calibrated trees were already widespread in phylogenetic literature.

Table 2.

Age of Brazilian Atlantic Rainforests (BAF) lineages of vascular plants based on phylogenetic literature and distribution data from Flora do Brasil [13] and Plants of the World Online [17]. ? refers to ages unavailable from the consulted literature.

Family Genus/Lineage BAF spp./Genus Phytophysiognomy Max Mean Min Reference
Ferns
Cyatheaceae Cyathea Sm. 23/290 Rainforest ? 30.0 ? [18]
Gymnosperms
Araucariaceae Araucaria Juss. 1/20 Rainforest ? 10.0 ? [19]
Podocarpaceae Podocarpus L’Hér. ex Pers. 2/115 Rainforest ? 15.0 ? [20]
Magnoliids
Annonaceae Hornschuchia Nees 10/10 Rainforest ? 20.0 ? [21]
Lauraceae Phyllostemonodaphne Koesterm. 1/1 Rainforest ? ? ? -
Lauraceae Urbanodendron Mez 3/3 Rainforest ? ? ? -
Monimiaceae Macropeplus Perkins 4/4 Rainforest ? 11.26 ? [22]
Monimiaceae Grazielanthus Peixoto and Per.-Moura 1/1 Rainforest ? 3.85 ? [22]
Monimiaceae Hennecartia J.Poiss. 1/1 Rainforest ? 15.58 ? [22]
Monimiaceae Macrotorus Perkins 1/1 Rainforest ? 11.26 ? [22]
Monimiaceae Mollinedia Ruiz and Pav. 32/55 Rainforest ? 2.20 ? [22]
Monocots
Amaryllidaceae Griffinia Ker Gawl. 17/22 Grassland ? ? ? -
Araceae Asterostigma Fisch. and C.A. Mey. 8/10 Rainforest ? ? ? -
Araceae Dracontioides Engl. 2/2 Rainforest ? ? ? -
Asparagaceae Herreria Ruiz and Pav. 6/8 Rainforest ? ? ? -
Bromeliaceae Alcantarea (E.Morren ex Mez) Harms 30/40 Rainforest 5.5 3.3 1.5 [23]
Bromeliaceae Araeococcus Brongn. 6/9 Rainforest ? 3.5 ? [24]
Bromeliaceae Billbergia Thunb. 35/63 Rainforest ? 4.5 ? [24]
Bromeliaceae Canistropsis (Mez) Leme 11/12 Rainforest ? 3.5 ? [24]
Bromeliaceae Stigmatodon Leme, G.K.Br. and Barfuss 18/18 Rainforest 6.4 5.5 2.8 [23]
Bromeliaceae Vriesea Lindl. 167/255 Rainforest 6.8 5.0 3.3 [23]
Commelinaceae Siderasis Raf. 6/6 Rainforest 16.69 8.57 2.26 [25]
Commelinaceae Dichorisandra J.C.Mikan 40/52 Rainforest 6.38 2.78 0.32 [25]
Dioscoreaceae Dioscorea L. 81/628 Rainforest 30.0 22.0 15.0 [26]
Iridaceae Neomarica Sprague 27/27 Grassland ? 6.5 ? [27]
Marantaceae Ctenanthe Eichler 11/15 Rainforest ? ? ? -
Marantaceae Maranta L. 20/37 Rainforest ? ? ? -
Marantaceae Saranthe Eichler 8/10 Rainforest ? ? ? -
Marantaceae Thalia L. 4/6 Rainforest ? ? ? -
Orchidaceae Bifrenaria Lindl. 17/21 Rainforest ? 13.0 ? [28]
Orchidaceae Capanemia Barb.Rodr. 6/9 Rainforest ? ? ? -
Orchidaceae Centroglossa Barb.Rodr. 6/6 Rainforest ? ? ? -
Orchidaceae Cirrhaea Lindl. 7/7 Rainforest ? ? ? -
Orchidaceae Hoehneella Ruschi 2/2 Rainforest ? ? ? -
Orchidaceae Isabelia Barb. Rodr. 3/3 Rainforest ? ? ? -
Orchidaceae Lankesterella Ames 7/11 Rainforest ? ? ? -
Orchidaceae Loefgrenianthus Hoehne 1/1 Rainforest ? ? ? -
Orchidaceae Miltonia Lindl. 19/19 Rainforest ? ? ? -
Orchidaceae Phymatidium Lindl. 9/9 Rainforest ? ? ? -
Orchidaceae Pseudolaelia Porto and Brade 10/15 Rainforest ? ? ? -
Poaceae Chusquea Kunth 45/185 Rainforest ? 9.0 ? [29]
Poaceae Merostachys Spreng. 44/53 Rainforest ? ? ? -
Poaceae Olyra L. 9/15 Rainforest ? 14.0 ? [30]
Poaceae Raddia Bertol. 9/12 Rainforest ? 22.0 ? [30]
Eudicots
Acanthaceae Herpetacanthus Nees 14/21 Rainforest ? ? ? -
Apocynaceae Bahiella J.F.Morales 2/2 Rainforest ? ? ? -
Apocynaceae Peplonia Decne. 8/13 Rainforest ? 13.0 ? [31]
Asteraceae Barrosoa R.M.King and H.Rob. 7/11 Rainforest ? ? ? -
Asteraceae Disynaphia Hook. and Arn. ex DC. 10/14 Rainforest ? ? ? -
Asteraceae Grazielia R.M.King and H.Rob. 7/12 Rainforest ? ? ? -
Asteraceae Pamphalea DC. 8/9 Rainforest ? ? ? -
Asteraceae Stifftia J.C.Mikan 4/6 Rainforest ? 34.0 ? [32]
Asteraceae Piptocarpha R.Br. 24/50 Rainforest ? ? ? -
Bignoniaceae Dolichandra Cham. 8/9 Rainforest 38.3 31.3 25.2 [33]
Bignoniaceae Paratecoma Kuhlm. 1/1 Rainforest ? ? ? -
Bignoniaceae Zeyheria Mart. 2/2 Rainforest ? ? ? -
Cactaceae Rhipsalis Gaertn. 37/43 Rainforest 11.82 7.67 4.26 [34]
Callophyllaceae Kielmeyera Mart. and Zucc. 24/50 Rainforest 23.0 15.54 10.0 [35]
Cleomaceae Tarenaya Raf. 14/14 Rainforest 18.39 16.60 14.7 [36]
Clusiaceae Tovomitopsis Planch. and Triana 2/2 Rainforest 34.0 20.46 13.0 [37]
Erythroxylaceae Erythroxylum P.Browne 71/259 Rainforest ? ? ? -
Euphorbiaceae Brasiliocroton P.E.Berry and Cordeiro 2/2 Rainforest 58.42 48.13 39.6 [38]
Euphorbiaceae Astraea Klotzsch 10/14 Rainforest 34.38 19.05 4.46 [38]
Euphorbiaceae Croton L. 98/1157 Rainforest 40.92 39.03 37.0 [38]
Fabaceae Dahlstedtia Malme 9/16 Rainforest ? ? ? -
Fabaceae Holocalyx Micheli 1/1 Rainforest 52.1 1.3 28.8 [39]
Fabaceae Moldenhawera Schrad. 8/11 Rainforest ? 48.0 ? [40]
Fabaceae Parapiptadenia Brenan 5/6 Rainforest ? 11.0 ? [41]
Fabaceae Paubrasilia Gagnon, H.C.Lima and G.P.Lewis 1/1 Rainforest ? 48.0 ? [41]
Fabaceae Schizolobium Vogel 1/1 Rainforest ? 40.5 ? [41]
Gentianaceae Calolisianthus (Griseb.) Gilg 4/4 Rainforest ? ? ? -
Gentianaceae Chelonanthus (Griseb.) Gilg 4/5 Rainforest ? ? ? -
Gentianaceae Deianira Cham. and Schltdl. 4/7 Rainforest ? ? ? -
Gentianaceae Prepusa Mart. 5/6 Rainforest ? ? ? -
Gentianaceae Senaea Taub. 1/2 Rainforest ? ? ? -
Gentianaceae Tetrapollinia Maguire and B.M.Boom 1/1 Rainforest ? ? ? -
Gesneriaceae Codonanthe (Mart.) Hanst. 8/9 Rainforest ? 7.0 ? [42]
Gesneriaceae Nematanthus Schrad. 32/32 Rainforest ? 7.0 ? [42]
Gesneriaceae Paliavana Vand. 4/6 Rainforest ? 7.0 ? [42]
Gesneriaceae Sinningia Nees 70/75 Rainforest ? 14.0 ? [42]
Gesneriaceae Vanhouttea Lem. 9/10 Rainforest ? 7.0 ? [42]
Loasaceae Blumenbachia Schrad. 7/12 Rainforest 4.22 27.5 20.7 [43]
Malpighiaceae Barnebya (Griseb.) W.R.Anderson and B.Gates 1/2 Rainforest ? 62.0 ? [44]
Melastomataceae Behuria Cham. 17/17 Rainforest ? 8.50 ? [45]
Melastomataceae Bertolonia Raddi 27/27 Rainforest ? 9.26 ? [45]
Melastomataceae Huberia DC. 13/17 Rainforest ? 8.50 ? [45]
Melastomataceae Physeterostemon R.Goldenb. and Amorim 5/5 Rainforest ? 2.50 ? [45]
Melastomataceae Pleiochiton Naudin ex A. Gray 12/12 Rainforest ? 4.43 ? [45]
Melastomataceae Pleroma D.Don 46/85 Rainforest ? 12.26 ? [45]
Moraceae Clarisia Ruiz and Pav. 2/2 Rainforest ? ? ? -
Moraceae Ficus L. 38/874 Rainforest ? 25.0 ? [46]
Myrtaceae Accara Landrum 1/1 Rainforest ? 32.0 ? [47]
Myrtaceae Blepharocalyx O.Berg. 3/4 Rainforest ? 40.0 ? [47]
Myrtaceae Calyptranthes Sw. 35/35 Rainforest ? 24.0 ? [47]
Myrtaceae Curitiba Salywon and Landrum 1/1 Rainforest ? 40.0 ? [47]
Myrtaceae Eugenia L. 254/1149 Rainforest ? 44.0 ? [47]
Myrtaceae Myrceugenia O.Berg. 33/45 Rainforest ? 25.0 ? [47]
Myrtaceae Myrcia DC. 200/609 Rainforest ? 28.0 ? [48]
Myrtaceae Myrciaria O.Berg. 18/27 Rainforest ? 26.0 ? [48]
Myrtaceae Myrrhinium Schott 1/1 Rainforest ? 29.0 ? [47]
Myrtaceae Neomitranthes D.Legrand 15/15 Rainforest ? 12.0 ? [47]
Myrtaceae Plinia L. 29/78 Rainforest ? 37.0 ? [47]
Myrtaceae Psidium L. 39/91 Rainforest ? 20.0 ? [47]
Rubiaceae Bathysa C. Presl 6/10 Rainforest ? ? ? -
Rubiaceae Bradea Standl. ex Brade 6/6 Rainforest ? ? ? -
Rubiaceae Coccocypselum P.Browne 14/22 Rainforest ? ? ? -
Rutaceae Conchocarpus J.C.Mikan 40/48 Rainforest ? ? ? -
Rutaceae Metrodorea A.St.-Hil 3/6 Rainforest ? ? ? -
Rutaceae Neoraputia Emmerich ex Kallunki 5/6 Rainforest ? ? ? -
Sapindaceae Cardiospermum L. 6/10 Rainforest ? 23.0 ? [49]
Sapindaceae Thinouia Triana and Planch. 7/11 Rainforest ? ? ? -
Solanaceae Petunia Juss. 10/16 Grassland 11.5 8.49 5.5 [50]
Vochysiaceae Callisthene Mart. 8/8 Rainforest 30.0 22.0 14.0 [51]
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Figure 4.

Figure 4

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Box plots summarizing the diversification of vascular plants through time in the Brazilian Atlantic Rainforest based on data presented in Table 2. (blue) Eudicots; (orange) Monocots; (gray)–Magnoliids; (yellow) Gymnosperms; (light blue) Ferns.

3. Discussion

3.1. Phylogenetics of Stigmaphyllon

The topology recovered from the combined dataset (i.e., ribosomal + nuclear markers) evidenced that the subgenera of Stigmaphyllon proposed by Anderson [10] are paraphyletic. All previous phylogenetic studies of Malpighiaceae sampled mostly Mesoamerican and Amazonian species of the genus [2,3,5,9,44], making it difficult to properly test the monophyly of its subgenera. The only BAF species of Stigmaphyllon sampled in previous studies were S. ciliatum and S. paralias. However, in all these studies S. paralias (a Brazilian Atlantic Rainforest lineage) is consistently recovered as sister to all remaining lineages of Stigmaphyllon. Additionally, this is the first time S. auriculatum, the type species of the genus, is included in a phylogenetic study. On the other hand, our results highly corroborate the previous topologies recovered for Stigmaphyllon, with the S. paralias group recovered as the first lineage to diverge, followed by the clade comprising the S. ciliatum group + S. subg. Ryssopterys sister to a large clade consisting of species from the S. tomentosum group (core Stigmaphyllon) [2,9]. Additional species sampling allied to a thorough morphological study on a phylogenetic perspective in Stigmaphyllon is urgently required to shed some light on its infrageneric classification.

3.2. Divergence Times and Biogeography of Stigmaphyllon

Our divergence times estimation for the MRCA of Stigmaphyllon (ca. 26.5 Mya) is similar to the age of 22.5 Mya estimated by Davis et al. [44] and of 21.0 Mya estimated by Willis et al. [9]. The estimated ages for the MRCAs obtained by us for the S. paralias group and the S. ciliatum + S. subg. Ryssopterys clade strongly corroborates those previously reported by Willis et al. [9] (17.0, 15.0, and 10.0 Mya, respectively). The only exception was the age of 19.0 Mya estimated by us for core-Stigmaphyllon when Willis et al. [9] recovered the estimation of 10.0 Mya for this clade. This apparent difference in age estimates might be due to the more comprehensive sampling of this clade in the present study.

Over these last 26.0 Mya, the lineages of Stigmaphyllon went through 13 dispersals and four vicariance events (VE). Worth noting is that VEs in this genus were always followed by a biome shifting event (BSE) from the BAFs to another tropical biome. The first VE followed by a BSE in Stigmaphyllon occurred ca. 15.0 Mya in the MRCA of S. urenifolium, from the BAFs to the Brazilian Cerrado. Several plant lineages present the same diversification pattern with older ancestors arising in the BAFs and colonizing the Cerrado biome ca. 15 Mya, such as clade 5 of Amphilophium Kunth (Bignoniaceae) [52], Astraea Klotzsch (Euphorbiaceae) [38], Dolichandra Cham. (Bignoniaceae) [33], Fridericia Mart. (Bignoniaceae) [52], and Xylophragma Sprague (Bignoniaceae) [53]. Dispersal events from forest to open habitats is one of the main factors explaining richness in Neotropical biodiversity [16]. Even though in Stigmaphyllon, those dispersal events occurred mostly among forested biomes, its single Cerrado lineage seems to point to an older diversification of this biome, such as in those from Vochysiaceae (20.0–15.0 Mya) [51]. Few species of Stigmaphyllon successfully colonized the Cerrado biome, such as S. jobertii, S. occidentale, S. tomentosum, and S. urenifolium. Future studies sampling those species in the molecular phylogeny of Stigmaphyllon are crucial to test if the genus colonized the Cerrado biome more than a single time. However, several studies seem to present the same pattern pointed by us of forest lineages occupying and diversifying in the Cerrado biome [16], with the opposite rarely recorded in biogeographic studies. We hypothesize that Cerrado lineages colonizing forested biomes might be rare due to the recent diversification of several plant lineages of Neotropical savannas [54].

The second VE followed by a BSE in Stigmaphyllon occurred ca. 12.0 Mya in the MRCA of S. sinuatum group, from the BAFs to the Amazon rainforest. The same pattern of diversification was recorded in other plant lineages, with Atlantic rainforest MRCAs colonizing the Amazon rainforest at this time, such as Eugenia L. clade G [55]. At least 50 dispersal events occurred between the Atlantic and Amazon rainforests [16]. The number of lineage exchanges between these biomes fluctuated over the last 60.0 Mya, with its previous increase starting ca. 12.0 Mya and peaking ca. 6.0–3.0 Mya [16], corroborating our results with Stigmaphyllon. The MRCA of S. finlayanum group was the fourth VE, followed by a BSE occurring in the genus, ca. 6.30 Mya, from the BAFs to the Amazon rainforest. The same pattern of diversification was recorded in other plant lineages, with Atlantic rainforest MRCAs colonizing the Amazon rainforest at this time, such as the clade 3 of Amphilophium Kunth (Bignoniaceae) [52] and the abovementioned study by Antonelli et al. [16].

The third VE followed by a BSE in Stigmaphyllon occurred ca. 10.0 Mya in the MRCA of S. subg. Ryssopterys + S. ciliatum group, from the BAFs to the Asian rainforests. This lineage diversified ca. 22.0 Mya, so we hypothesize that its MRCA was widely distributed among dunes vegetation in the Atlantic and Asian rainforests via the Antarctic route. Antarctica’s glaciation process started ca. 34.0 Mya, during the Eocene/Oligocene transition, on high altitude regions of this continent [56]. From 34.0–12.0 Mya, Antarctica had intermittent ice sheet coverage, leaving intact Tertiary pockets of pre-glaciation fauna and flora that only went completely extinct ca. 12.0 Mya with the formation of permanent ice sheets in this continent [57], the same confidence interval recovered in our study for the MRCA of S. subg. Ryssopterys + S. ciliatum group. The same pattern of vicariance event is observed in the Drymophila (Australian) + Luzuriaga (South American) clade (Alstromeriaceae), in which its MRCA split ca. 23.0 Mya, giving rise to these genera from ca. 10.0 to 4.0 Mya [58].

On the other hand, 14 dispersal events (DE) occurred within Stigmaphyllon, mostly within the North-South corridors of the BAFs, and at least three DEs from the BAFS to the Caatinga biome. From these latter three DEs, the first occurred ca. 14.0 Mya in the MRCA of S. paralias group, the second occurred ca. 9.0 Mya in the MRCA of S. saxicola group and the third occurred ca. 1.0 Mya in the MRCA of the S. auriculatum group. From the remaining DEs that happened within the BAFs, at least five of them occurred from North to South ca. 22.0, 17.0, 12.0, 11.0, and 9.0 Mya. The same pattern with Northern BAF lineages colonizing Southern portions of this biome is observed in Aechmea (Bromeliaceae) [59]. However, the North-South dispersals in this genus started only ca. 6.0 Mya (Bromeliaceae) [59], being much younger than those in Stigmaphyllon.

3.3. Time and Diversification of the Atlantic Rainforest

Several implications for understanding the BAFs historical biogeography might be postulated from the biogeographical study of Stigmaphyllon. Our results suggest a late-Eocene origin for these forests, that seems to be partially corroborated by the literature. Until the late Paleocene and early Eocene, the Earth’s climate was mostly warmer and more humid than today, suggesting that South America was probably covered by continuous rainforests [60,61]. When comparing the mean ages recovered in published studies for several lineages of ferns, gymnosperms, and angiosperms diversified in the BAFs, we bring new evidence that vascular plants started colonizing these forests over the last 60.0 Mya (Figure 4; Table 2), corroborating the abovementioned authors. The oldest lineage to occupy the BAFs might have been the genus Barnebya W.R.Anderson and B.Gates ca. 60 Mya (Malpighiaceae, Eudicots), with the diversification of most Eudicot lineages in these forests occurring from 40.0 to 15.0 Mya (Figure 4; Table 2). During the late Eocene and Oligocene, global episodes of cooling and dryness favored the expansion of grasslands in the southern and central regions of the continent [60,62], which culminated in the formation of a diagonal belt of more open and drier biomes (also known as “dry diagonal”) [63]. The formation of the dry diagonal marked the formation of the Atlantic forest in the east and Amazonia in the west [64]. On the other hand, the colonization and diversification of Magnoliid lineages took place from 18.0 to 3.0 Mya (Figure 4; Table 2), followed by gymnosperm lineages that diversified from 15.0 to 11.0 Mya, and finally from monocot lineages diversifying from 12.0 to 3.0 Mya in these rainforests (Figure 4; Table 2). Fossil records and paleoclimate studies suggest that the BAFs and the Amazon rainforests were re-connected multiple times in the Miocene and Pliocene [64]. Mean ages regarding the colonization and diversification of ferns in the BAFs are still incipient, with a single study on the family Cyatheaceae evidencing its initial diversification in these forests at 30.0 Mya (Figure 4; Table 2). Additionally, from the 113 BAF lineages presented in Table 2, only 64 show mean ages based on time-calibrated phylogenies available in the literature. At least 18 families of angiosperms (Acanthaceae, Amaryllidaceae, Apocynaceae, Araceae, Asparagaceae, Asteraceae, Bignoniaceae, Erythroxylaceae, Fabaceae, Gentianaceae, Lauraceae, Marantaceae, Moraceae, Orchidaceae, Poaceae, Rubiaceae, Rutaceae, and Sapindaceae) with lineages diversified in the Atlantic forest still lack published time-calibrated phylogenies.

Another worth mentioning factor that might have played an important role in the diversification of the BAFs was the uplift of Serra do Mar and Serra da Mantiqueira Mountain Ranges in Eastern Brazil. Those mountains were previously thought to have uplifted around 120.0 Mya, but geological studies from the past decade have pointed to an earlier uplifting age for these mountains, from 60.0 to 30.0 Mya [65]. The tertiary uplift age of these mountains in Eastern Brazil was a direct result of the Andean uplift, coinciding with our results for the colonization of the BAFs by 64 lineages of vascular plants [65].

4. Material and Methods

4.1. Taxon Sampling and Plant Material

We sampled 24 species of Stigmaphyllon (ca. ¼ of the Neotropics’ genus diversity: 18 spp. from the Brazilian Atlantic Rainforest (out of 31 spp.), three spp. from the Amazon Rainforest, two spp. from the Caatinga, and one spp. from the Cerrado biomes), including outgroups Bronwenia W.R.Anderson and C.C.Davis and Diplopterys A.Juss. From this total, 23 species represent S subg. Stigmaphyllon and a single species [Stigmaphyllon timoriense (DC) C.E.Anderson] represents S. subg. Ryssopterys (Table 3). For DNA extraction, we used mainly field-prepared silica dried leaves (12–80 mg) and herbarium specimens as necessary (Table 3).

Table 3.

Species and DNA regions sampled in this study. Genbank accession numbers are presented for columns ETS (External Transcribed Spacer), ITS (Internal Transcribed Spacer), and PHYC (Phytochrome C gene). * Sequences were obtained from GenBank.

Species Voucher (Herbarium Acronym) ETS ITS PHYC
Bronwenia cinerascens (Benth.) W.R.Anderson and C.C.Davis Nee 48, 658 (SP) KR054586.1 HQ246821.1 * HQ246987.1 *
Diplopterys pubipetala (A.Juss.) W.R.Anderson and C.C.Davis Francener 1126 (SP) KR092986 HQ246821.1 * HQ247045.1 *
Stigmaphyllon alternifolium A.Juss. Almeida 501 (SP) KR054612.1 - -
Stigmaphyllon angustilobum A.Juss. Almeida 503 (SP) KR054591.1 MT559811 -
Stigmaphyllon arenicola C.E.Anderson Sebastiani 5 (SP) KR054589.1 - -
Stigmaphyllon auriculatum (Cav.) A.Juss. Almeida 584 (HUEFS) KR054592.1 MT559812 -
Stigmaphyllon blanchetii C.E.Anderson Almeida 525 (SP) KR054615.1 MT559813 -
Stigmaphyllon bonariense A.Juss. Queiroz 13, 530 (HUEFS) KR054607.1 - -
Stigmaphyllon caatingicola 1 R.F.Almeida and Amorim Almeida 577 (HUEFS) KR054595.1 MT559814 -
Stigmaphyllon caatingicola 2 R.F.Almeida and Amorim Almeida 629 (HUEFS) MT490608 MT559815 -
Stigmaphyllon cavernulosum C.E.Anderson Cardoso 2083 (HUEFS) KR054609.1 - -
Stigmaphyllon ciliatum (Lam.) A.Juss. Almeida 541 (SP) KR054590.1 - HQ247151.1 *
Stigmaphyllon finlayanum A.Juss. Pace 457 (SPF) KR054599.1 - HQ247152.1 *
Stigmaphyllon gayanum A.Juss. Almeida 500 (SP) KR054610.1 - -
Stigmaphyllon harleyi C.E.Anderson Santos 378 (HUEFS) KR054594.1 MT581513 -
Stigmaphyllon jatrophifolium A.Juss. Filho s.n. (SP369102) KR054614.1 - -
Stigmaphyllon lalandianum A.Juss. Kollmann 4279 (CEPEC) KR054596.1 - -
Stigmaphyllon lindenianum A.Juss. Aguillar 718 (SP) KR054603.1 - HQ247153.1 *
Stigmaphyllon macropodum A.Juss. Almeida 538 (SP) KR054602.1 MT559816 -
Stigmaphyllon paralias A.Juss. Almeida 509 (SP) KR054593.1 KY421909.1 AF500566.1 *
Stigmaphyllon puberulum A.Juss. Perdiz 732 (HUEFS) KR054600.1 - -
Stigmaphyllon salzmannii A.Juss. Almeida 526 (SP) KR054616.1 MT559817 -
Stigmaphyllon saxicola C.E.Anderson Badini 24,261 (HUEFS) KR054605.1 MT559818 -
Stigmaphyllon sinuatum (DC.) A.Juss. Amorim 3159 (CEPEC) KR054608.1 - -
Stigmaphyllon timoriense (DC) C.E.Anderson Anderson 796 (US) - - AF500545.1 *
Stigmaphyllon urenifolium A.Juss. Guedes 13,932 (HUEFS) KR054604.1 - -
Stigmaphyllon vitifolium A.Juss. DalCol 233 (HUEFS) KR054598.1 - -
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4.2. Molecular Protocols

Genomic DNA was extracted using the 2 × CTAB protocol, modified from Doyle and Doyle [66]. Three DNA regions (nuclear PHYC gene, and the ribosomal external and internal transcribed spacers (ETS and ITS)) were selected based on their variability in previous Malpighiaceae studies [2,5,6,8,67]. Protocols to amplify and sequence ETS and ITS followed Almeida et al. [8]. For amplification, we used the TopTaq (Qiagen) mix following the manufacturer’s standard protocol, with the addition of betaine (1.0 M final concentration) and 2% DMSO for the ETS region. PCR products were purified using PEG (polyethylene glycol) 11% and sequenced directly with the same primers used for PCR amplification. Sequence electropherograms were produced on an automatic sequencer (ABI 3130XL genetic analyzer) using the Big Dye Terminator 3.1 kit (Applied Biosystems). Additional sequences for PHYC were retrieved from GenBank (Table 3). Newly generated sequences were edited using the Geneious software [68], and all datasets were aligned using Muscle [69], with subsequent adjustments in the preliminary matrices made by eye. The complete data matrices are available at TreeBase (accession number S21218). This study was authorized by the Genetic Heritage and Associated Traditional Knowledge Management National System of Brazil (SISGEN #A3B8F19).

4.3. Phylogenetic Analysis

Analyses were rooted in Bronwenia, according to Davis and Anderson [2]. Individual analyses for each marker were performed, and since no significant incongruencies were found, analyses of combined matrices (i.e., nuclear + ribosomal markers) were performed using maximum parsimony (MP) conducted with PAUP 4.0b10a [70]. A heuristic search was performed using TBR swapping (tree-bisection reconnection), and 1000 random taxon-addition sequence replicates with TBR swapping limited to 15 trees per replicate to prevent extensive searches (swapping) in suboptimal islands, followed by TBR in the resulting trees with a limit of 1000 trees. In all analyses, the characters were equally weighted and unordered [71]. Relative support for individual nodes was assessed using non-parametric bootstrapping [72], with 1000 bootstrap pseudoreplicates, TBR swapping, simple taxon addition, and a limit of 15 trees per replicate.

For the model-based approach, we selected the model GTR + I + G using hierarchical likelihood ratio tests (HLRT) on J Modeltest 2 [73]. A Bayesian analysis (BA) was conducted with mixed models and unlinked parameters, using MrBayes 3.1.2 [74]. The Markov chain Monte Carlo (MCMC) analysis was performed using two simultaneous independent runs with four chains each (one cold and three heated), saving one tree every 1000 generations for a total of ten million generations. We excluded as ‘burn-in’ trees from the first two million generations, and tree distributions were checked for a stationary phase of likelihood. The posterior probabilities (PP) of clades were based on the majority-rule consensus produced with the remaining trees in MrBayes 3.1.2 [74].

4.4. Calibration

Estimates were conducted based on a simplified ultrametric Bayesian combined tree generated with BEAST 1.8.4 [75]. This analysis used a relaxed uncorrelated lognormal clock and Yule process speciation prior to inferring trees. The calibration parameters were based on previous estimates derived from a comprehensive fossil-calibrated study of the whole Malpighiaceae [44,76]. We opted for calibrating at the root, using a normal prior with mean initial values of 40.0 Mya (representing the age estimated for the MRCA of the Stigmaphylloid clade) and a standard deviation of 1.0 [44,67,76]. Two separate and convergent runs were conducted, with 10,000,000 generations, sampling every 1000 steps, and 2000 trees as burn-in. We checked for ESS values higher than 400 for all parameters on Tracer 1.6 [77]. Tree topology was assessed using TreeAnnotator and FigTree 1.4.0 [78].

4.5. Ancestral Area Reconstruction

Species distribution data were compiled from the taxonomic revision of Bronwenia [79], Diplopterys [80], and Stigmaphyllon [10,11] (Figure 3). Occurrences were categorized according to a modified version of the biome domains adopted by IBGE [81] and WWF [82], which reflects distribution patterns in Stigmaphyllon, namely: (A) Brazilian Atlantic Rainforest, (B) Seasonally Dry Tropical Forest [Caatinga], (C) Amazon Rainforest, (D) Cerrado, and (E) Australasian Rainforests (Figure 2). Ancestral areas of Stigmaphyllon and its relatives were estimated using a maximum likelihood analysis of geographic range evolution using software Rasp 3.2 [83]. Estimates were conducted using the statistical dispersal-extinction-cladogenesis (S-DEC) [84], according to the parameters proposed by Ree and Sanmartín [85].

4.6. Meta-Analysis

Ages of BAF lineages of vascular plants (ferns/lycophytes, gymnosperms, magnoliids, monocots, and eudicots) were compiled based on the phylogenetic literature and distribution data from Flora do Brasil [12] and Plants of the World Online [17]. Online repositories such as GBIF, BIEN and Species Link were not used since specimen identification is not usually updated or are not identified by a Malpighiaceae specialist. Additionally, the main problem in using all the above-mentioned repositories is that only Flora do Brasil present reliable information on the biome distribution of species sampled in our study. We considered a genus or lineage within a genus diversified in the BAF when at least 50% of its total number of species occurred in this biome. Data from BAF lineages of vascular plant species are presented in Table 2, alongside estimated ages, and references. A boxplot graphic is also presented in Figure 4, showing the diversification of vascular plants through time in the BAF based on data presented in Table 2.

5. Conclusions

Even though dispersal events from forested to open habitats have been recently identified as one of the main factors explaining richness in Neotropical biodiversity [16], the same pattern was not recovered for Stigmaphyllon. A late-Eocene origin for this genus is suggested, with its MRCA originating in the Northeastern BAFs, with several dispersal events taking place to other Neo- and Paleotropical biomes from 22.0 to 1.0 Mya, alongside several dispersals from Northern to Southern portions of the BAFs. When comparing our results with published divergence times for BAFs’ vascular plant lineages, a late-Eocene origin for these forests was evidenced. The immense gap in time-calibrated phylogenies focusing on BAFs’ vascular plant lineages is still the most significant impediment for a more comprehensive understanding of the plant diversification timeframe in these forests. Additionally, the recent evidenced tertiary uplift of Serra do Mar and Serra da Mantiqueira Mountain Ranges might also have played an important role in the diversification of the megadiverse BAFs.

Acknowledgments

We thank the staff and curators of all herbaria for their assistance with loans and DNA samples; Marco Octávio de Oliveira Pellegrini for valuable suggestions on an early version of the manuscript and review of the English language; and three anonymous reviewers for valuable comments during the reviewing process.

Author Contributions

Conceptualization, R.F.d.A.; methodology, R.F.d.A., and C.v.d.B.; software, R.F.d.A.; validation, R.F.d.A., and C.v.d.B.; formal analysis, R.F.d.A., and C.v.d.B.; investigation, R.F.d.A., and C.v.d.B.; resources, R.F.d.A. and C.v.d.B.; data curation, R.F.d.A.; writing—original draft preparation, R.F.d.A., and C.v.d.B.; writing—review and editing, R.F.d.A. and C.v.d.B.; visualization, R.F.d.A. and C.v.d.B.; supervision, C.v.d.B.; project administration, C.v.d.B.; funding acquisition, C.v.d.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by CNPq, grant number #309880/2013-0, Smithsonian Institution, Cuatrecasas award, and FAPESB, grant number #PNX0014/2009.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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