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. 2017 May 30;7(13):4919–4935. doi: 10.1002/ece3.3036

Molecular genetic analysis of two native desert palm genera, Washingtonia and Brahea, from the Baja California Peninsula and Guadalupe Island

Anastasia Klimova 1,2, Joseph I Hoffman 2,✉, Jesus N Gutierrez‐Rivera 1, Jose Leon de la Luz 1, Alfredo Ortega‐Rubio 1
PMCID: PMC5496553  PMID: 28690819

Abstract

The complex geological and ecological processes that have generated high levels of biodiversity and endemism in the Baja California Peninsula have been the subject of intensive study. However, relatively little is known about phylogeography of the iconic endemic palm species of this region. We therefore analyzed a total of 2,294 bp of chloroplast and 738 bp of nuclear sequence data in 169 samples of five native palm species from Baja California, Sonora and Guadalupe Island. We found that Washingtonia and Brahea palms had low levels of genetic diversity and were highly structured, with the majority of species and major geographic regions being characterized by distinct haplotypes. We also found strong support for currently recognized species in Washingtonia, but our results were less clear cut for Brahea due to haplotype sharing. Furthermore, patterns of population structure were broadly consistent with historical vicariant events such as the inundation of the Isthmus of La Paz, the formation of the Sea of Cortez, and the more recent colonization and isolation of Guadalupe Island's palms. Our findings contribute toward a growing appreciation of the complexity of plant responses to past geological changes and also provide valuable baseline genetic data on relict American palm species.

Keywords: Baja California Peninsula, desert fan palms, relict species, species distributions

1. INTRODUCTION

Spatial patterns of species abundance and distribution are of a fundamental importance as they contribute toward virtually every facet of ecological knowledge from conservation to the understanding of ecosystem function and structure. Current species distributions arise from the interplay of various evolutionary, ecological and geological forces as well as from stochastic effects acting on species and populations. Multiple factors have been implicated in shaping species distributions including contemporary climate conditions (Currie et al., 2004; Svenning & Skov, 2007), Quaternary climatic oscillations (Hewitt, 1996, 2000, 2004), topography and habitat heterogeneity (Kerr & Packer, 1997), dispersal capacity (Svenning, Normand, & Skov, 2008), and biotic interactions (Araújo & Luoto, 2007; Kissling, Rahbek, & Bohning‐Gaese, 2007).

The biological diversity of the Baja California Peninsula has long been recognized as unique and significant (Grismer, 2000; Lindell, Ngo, & Murphy, 2006; Riemann & Ezcurra, 2005; Wiggins, 1980). The Baja California is also considered a “natural laboratory” in which multiple geological and ecological events are thought to have triggered cycles of vicariant episodes followed by dispersion along climatic gradients (Mantooth, Hafner, Bryson, & Riddle, 2013; Riddle, Hafner, Alexander, & Jaeger, 2000). The major geological processes that have been evoked in explaining patterns of biotic diversification in the region have been classified on the basis of their timing and strength (Dolby, Bennett, Lira‐Noriega, Wilder, & Munguia‐Vega, 2015). The continental rifting of the Peninsula away from mainland Mexico and the volcanic upwelling of Guadalupe Island are the most ancient (>5 million years ago, MYA) and resulted in ecological speciation, island endemism and disjunctions in mainland‐peninsular and peninsular‐island sister species distributions (Aleixandre, Hernandez Montoya, & Mila, 2013; Grismer, 2000; León De La Luz, Rebman, & Oberbauer, 2003; Riddle et al., 2000; Rosas‐Escobar, Gernandt, Pinero, & Garcillan, 2011). More recently (1–3 MYA) and more locally, complex physical interactions between the land and the sea, such as the inundation of the Isthmus of La Paz and the formation of the temporal mid‐peninsular seaway, resulted in a north‐south genetic discontinuity within the peninsula and the generation of regions of high local endemism (Dolby et al., 2015; León‐De la Luz & Breceda, 2006; McCauley, Cortés‐Palomec, & Oyama, 2010; Riddle et al., 2000). This complex interplay was followed by progressive aridification of the Baja Peninsula and adjacent areas after the Last Glacial Maximum (LGM) (Hafner & Riddle, 1997; Lindell et al., 2006; Riddle et al., 2000). Following drastic changes in precipitation, a number of endemic species are thought to have become either locally extinct or restricted to isolated permanent water bodies such as oases and canyons (Grismer & McGuire, 1993; Wehncke, López‐Medellín, & Ezcurra, 2010).

Palms (Arecaceae) are one of the most distinctive of all plant families and are emblematic of the tropics (Tregear, Rival, & Pintaud, 2011). Although the majority of palm species are restricted to the wet tropics, several groups occur in dry open savannas and desert oases (Tomlinson, 2006). Palm populations on the Baja California Peninsula are considered to be relicts of historically more widespread and continuous populations that are now largely confined to sites where permanent water exists either above or below the ground (Axelrod, 1950; Cornett, 1985; Cornett, Glen, & Stewart, 1986; Felger & Joyal, 1999; Grismer & McGuire, 1993). This is evident in the fossil record, which shows that during the late Cretaceous, palms were common across North America and extended much further than their current geographic distribution (Couvreur, Forest, & Baker, 2011; Harley, 2006).

Two native palm genera (Washingtonia spp. and Brahea spp.) are currently present on the Baja Peninsula (Minnich, Franco‐Vizcaino, & Salazar‐Ceseña, 2011). The genus Washingtonia is represented by two species, W. robusta and W. filifera, but the taxonomical relationships within this genus are poorly resolved (Felger & Broyles, 2007; Felger & Joyal, 1999; Henderson, Galeano, & Bernal, 1995; McClintock, 1978). W. filifera is distributed from southeastern California and western Arizona to northern Baja California (McClintock, 1978). By contrast, W. robusta is locally distributed near Cataviña and Sierra Asamblea and is more common in the southern half of the Baja peninsula (Minnich et al., 2011). It also occurs on the Mexican mainland, where it is restricted to a few riparian canyons at the southern edge of the Sonoran Desert and appears to be relictual, being geographically and ecologically the most narrowly distributed palm species in the region (Felger & Joyal, 1999). There is still unresolved debate over the relictual status of Washingtonia palms, with some authors having suggested that their current distribution is of recent invasive origin (Cornett, 1987b, 2008) or might be linked to the movement of native human populations (Hicks, 1989; Minnich et al., 2011). One the other hand, many characteristics of Washingtonia palms such as their patchy geographical distributions, low numbers, and affinity to tropical climates would support fossil evidence in suggesting that their current distribution may be relictual (Axelrod, 1950; Felger & Joyal, 1999).

The Brahea complex comprises nine species, two of which are endemic and restricted to Baja California (B. brandegeei and B. armata) and one (B. edulis) to Guadalupe Island. The remaining Brahea species are absent from the Baja California Peninsula but can be found on the Mexican mainland, with some species (B. nitida and B. dulcis) extending their range into Central America. Brahea is the least studied genus of American palms and the relationships between and within its species are not clearly described (Henderson et al., 1995). The geographical range of B. brandegeei extends from the northern Baja California Sur (Sierra San Francisco) to Sierra La Laguna at the southernmost tip of the peninsula (Felger, Johnson, & Wilson, 2001; Minnich et al., 2011). B. armata extends from just south of the United States‐Mexico border southward to just north of the state line of Baja California Sur in the central peninsula (Franco‐Vizcaino, Lopez‐Beltran, & Salazar‐Cesena, 2007; Wiggins, 1980). Nonetheless, the exact limits of the ranges of B. armata and B. brandegeei are unclear because of taxonomic uncertainties (Felger & Joyal, 1999; Felger et al., 2001; Henderson et al., 1995). The Guadalupe fan palm or B. edulis is distributed across the northwestern side of Guadalupe Island (Garcillán, Vega, & Martorell, 2012; León De La Luz et al., 2003) with small patches found along the bottoms of arroyos throughout the island (Oberbauer, 2005).

In spite of the ecological, ethno‐biological and economical importance of Washingtonia and Brahea palms, many aspects of their biology including species delimitations, genetic relationships between species and levels of intraspecific genetic diversity remain to be elucidated. Previous studies have examined certain aspects of the fundamental ecology of these species such as growth rates, mechanisms of seed dispersal and herbivore–plant interactions (Bullock & Heath, 2006; Franco‐Vizcaino et al., 2007; Wehncke & López‐Medellín, 2015; Wehncke, López‐Medellín, Wall, & Ezcurra, 2013; Wehncke et al., 2010). The geographic distributions of certain species based on morphological characteristics such as stem size, leaf shape and color, fruit shape and size, have also been described (Cornett 2008; Felger & Joyal, 1999; Oberbauer, 2005; Minnich et al., 2011). However, because morphological differences can sometimes be ambiguous and the majority of Washingtonia and Brahea populations on the peninsula are extremely hard to access (Felger & Joyal, 1999) no single study has effectively elucidated the distribution of all of the palms found in the Baja California Peninsula and Guadalupe Island.

In recent decades, molecular genetic studies have proven instrumental in resolving ongoing debates over the biogeographical origins of diverse taxa, including the Aracaceae (Baker & Couvreur, 2013; Couvreur et al., 2011; Kissling, Baker, et al., 2012, 2012; Kissling, Eiserhardt, et al., 2012, 2012; Kondo et al., 2012). However, the majority of studies of palms have focused on commercially important species (Barrett, Bacon, Antonelli, Cano, & Hofmann, 2016) and we are not aware of any published genetic studies of Washingtonia or Brahea species, with the exception of a single allozyme study of W. filifera in California (McClenaghan & Beauchamp, 1986).

Here we used Washingtonia and Brahea palms as a case study to explore how tropical species may have responded to the complex geological and ecological history of the mostly arid Baja California Peninsula and adjacent Guadalupe Island. These genera share similar life histories and habitat requirements yet both occupy the northern limit of the Arecaceae distributional range, are endemic and locally rare. To provide the first baseline genetic data on Washingtonia and Brahea palms from this region, we used a classical Sanger sequencing approach. By combining chloroplast and nuclear sequence data, we first set out to determine species delimitations on the Baja Peninsula. We then characterized patterns of haplotype diversity and distribution to address a number of questions: (i) Do sympatrically occurring Washingtonia and Brahea palms exhibit similar patterns of genetic structure along the Baja Peninsula? (ii) Is the restricted distribution of desert palms reflected in low genetic diversity and high divergence between major geographic regions? (iii) Are patterns of geographically structured genetic variation concordant with major historical vicariant events that shaped the region such as the formation of the Gulf of California, the inundation of the Isthmus of La Paz and the formation of Guadalupe Island?

2. MATERIALS AND METHODS

2.1. Sampling

A total of 176 samples were collected from a total of five palm species (Washingtonia and Brahea) identified on the basis of their morphology in the field. Specimens were collected from virtually all accessible oases throughout the Baja California Peninsula as well as from Guadalupe Island and two sites in Sonora, Mexico (Figure 1). We avoided sampling immediately adjacent trees in order not to include close relatives in our dataset. Although our total sample size is modest, it is important to note that the species in question are rare and endemic, and normally grow in inaccessible canyons. Many sites could only be reached by foot or by riding a mule for several hours and in some cases days. Additionally, some stands were very small and were represented by only 5–10 individuals. The full distributional ranges of W. robusta, B. armata, B. edulis, and B. brandegeei were covered, although W. filifera was represented by samples only from Mexico. In total we collected 91 Washingtonia samples from eight populations (sierras), of which eight samples corresponded to W. filifera and 83 to W. robusta. For Brahea, we collected 85 samples from nine populations (sierras) and tenth popilation from Guadalupe Island, of which 17 samples belonged to B. edulis, 29 to B. armata and 39 to B. brandegeei. As some authors (e.g., Henderson et al., 1995) have argued that B. brandegeei may be synonymous to B. elegans from the Mexican mainland, we also included one herbarium specimen of this species. More details on sampled species, sierras and sites, and the number of amplified chloroplast and nuclear sequences can be found in Figure 1, Tables 1 and S1. The genetic data were generated from silica‐gel dried leaf samples collected in the field during 2015 and 2016.

Figure 1.

Figure 1

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Map showing the sampling sites of Washingtonia spp. and Brahea spp. used in our study. The sampling and distributional limits of W. filifera were restricted only to the Mexican populations in Sierra Juarez. Abbreviations correspond to the names of the sampled sierras (populations): SL, Sierra La Laguna; SM, Sierra Mechudo; SG, Sierra Giganta; SSP, Sierra San Pedro; SSF, Sierra San Francisco; SLI, Sierra Libertad; SA, Sierra Asamblea; Cat, Cataviña; SSPM, Sierra San Pedro Martir; SJ, Sierra Juarez; GI, Guadalupe Island and SON, Mexican mainland

Table 1.

Numbers of Washingtonia and Brahea samples collected and successfully sequenced at nuclear and plastid loci. Also shown are the number of population sampled for each species and sampling sites are included for each population and species. The sampled populations (sierras) correspond to those shown in Figure 1

Species Sierra (Population) Number of sampling sites in each Sierra Number of collected samples per population Number of sequences amplified
Nuclear( )738 bp Chloroplast 2,294 bp
W  robusta Cabo Region (SL) 5 16 16 11
Sierra Mechudo (SM) 9 28 28 26
Sierra La Giganta (SG) 5 12 12 12
Sierra San Pedro (SSP) 1 4 4 3
Sierra Aguaje (Son) 2 10 10 9
San Fransisco de la Sierra (SSF) + Sierra Libertad (SLI) 2 8 7 7
Cataviña (Cat) 2 5 5 5
W. filifera Sierra Juárez (SJ) 3 8 7 8
Total Washingtonia 29 91 89 81
B. brandegeei Cabo Region (SL) 7 18 18 17
Sierra Mechudo (SM) 3 9 9 8
Sierra San Pedro (SSP) 1 5 5 3
San Fransisco de la Sierra (SSF) 2 7 6 7
B. armata Sierra Libertad (SLI) 3 7 7 7
SierraAsamblea (SA) 1 4 4 2
Cataviña (Cat) 2 5 5 5
Sierra San Pedro Mártir (SSPM) 4 7 5 7
Sierra Juárez (SJ) 2 6 6 6
B. edulis Guadalupe Island (GI) 3 17 14 17
B. elegans Sonora (BEL) 1 1 1 1
Total Brahea 29 86 80 80
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2.2. Molecular techniques

DNA extraction was performed using QIAGEN DNeasy plant mini kit (Valencia, CA, USA). As we are unaware of any population‐level genetic studies of Washingtonia or Brahea, we first evaluated three nuclear and seven chloroplast loci that have previously been used in phylogenetic and biogeographic studies of Arecaceae (Bacon, Baker, & Simmons, 2011; Bacon, Feltus, Paterson, & Bailey, 2008; CBOL Plant Working Group 2009; Jeanson, Labat, & Little, 2011; Shaw et al., 2005; Taberlet, Gielly, Pautou, & Bouvet, 1991). These loci (ITS 2, CISP 4, CISP 8, matK, rbcl, trnT‐trnD, trnG‐trnS, trnC‐rpoB, trnF‐trnL, trnfM‐trnS) were selected based on the amount of intrageneric diversity they possess in other plant species. For this trial, 40 samples of five palm species were PCR amplified in a 12.5 μl reactions containing 50–100 ng of DNA template, 1× PCR buffer, 1.5 mM MgCl2, 200 mM of dNTP mix, 0.4 mM of each primer, and 0.5 U of GoTaq Flexi DNA polymerase (Promega). The loci were amplified using primers and thermocycling protocols described elsewhere (Bacon et al., 2008; Jeanson et al., 2011; Shaw et al., 2005; Taberlet et al., 1991). Five loci (one nuclear and four chloroplast) were deemed suitable for further study and these were sequenced in all of the samples using the PCR conditions described above. The presence of amplified target DNA fragments was verified on 1.5% agarose gels stained with ethidium bromide. All positive PCR products were sent to Arizona GeneCore for sequencing in both directions. The resulting sequence chromatograms were assembled and manually edited using BioEdit 7.0.0 (Hall, 1999). The chloroplast sequences were then concatenated into a single sequence, as were the nuclear sequences, allowing subsequent analyses to be carried out separately for these two types of loci.

2.3. Molecular data analysis

Our sample size was somewhat restricted due to the difficulty of collecting samples from these locally rare and geographically restricted endemic species. We therefore tested if our final sample size was sufficient to recover most of the genetic diversity within the sampled populations. For this analysis, we constructed haplotype accumulation curves separately for the nuclear and chloroplast sequence data using the function haploAccum in the R package SPIDER (R Development Core Team 2008) with a total of 10,000 permutations. Molecular diversity statistics including the number of variable sites, the number of haplotypes, nucleotide and haplotype diversities, and the number of shared haplotypes were then computed using DnaSP 5.1 (Librado & Rozas, 2009) and ARLEQUIN 3.5.1.3 (Excoffier & Lischer, 2010). Phylogenetic relationships among the samples were inferred on the basis of the nuclear and chloroplast sequence data by constructing a parsimony network (Clement, Posada, & Crandall, 2000; Templeton, Crandall, & Sing, 1992) in PopArt (http://popart.otago.ac.nz, June 2016). We also used Gengis 2.1.1 (Parks et al., 2009) to visualize plastid and nuclear sequence geographic distributions.

To assess levels of genetic divergence between putative taxonomic species and a priori defined geographical regions (Figure 1, Table 1 and see below), we quantified pairwise differentiation using F st (Weir & Cockerham, 1984) and Φst (Kimura, 1980). The former looks only at haplotype frequency differences (Excoffier, Smouse, & Quattro, 1992) while the latter also incorporates haplotype sequence similarity. F st and Φst values were calculated within ARLEQUIN. For Washingtonia, eight geographic regions, each corresponding to a different sierra, were defined as follows: Mexican mainland (Son), Cabo Region (inluding Sierra La Laguna combined with Sierra Cacachilas, SL), Sierra del Mechudo (SM), Sierra la Giganta (SG), Sierra San Pedro (SSP), combined sites of Sierra Libertad and Sierra San Francisco (SLI + SSF), Cataviña (Cat) and Sierra Juárez (SJ). For Brahea, we specified ten geographical regions. Nine of these corresponded to different sierras on the Baja Peninsula: Cabo Region (SL), Sierra del Mechudo (SM), Sierra San Francisco (SSF), Sierra San Pedro (SSP), Sierra Libertad (SLI), Sierra Asamblea (SA), Cataviña (Cat), Sierra San Pedro Martir (SSPM) and Sierra Juárez (SJ); while the final geographical region corresponded to Guadalupe Island (GI). For further details including sampling coordinates, see Tables 1 and S1; Figures S1 and S2.

We also used hierarchical analysis of molecular variance (AMOVA) to partition the genetic variation within Washingtonia and Brahea using ARLEQUIN. We used AMOVA to estimate relative support for three alternative scenarios (Figure 2). Each scenario specified a hierarchical partitioning of populations within regions/groups, and the nesting scheme that maximized the among‐group variance component was considered the best divergence scenario. The first scenario was based on the current taxonomical delimitation of the species (i.e. two groups were specified for Washingtonia, corresponding to W. filifera and W. robusta and three groups were specified for Brahea corresponding to B. edulis, B. armata, and B. brandegeei). Second, for the Washingtonia palms, we constructed a scenario based on the isolation of the mainland and peninsular populations after the formation of Sea of Cortez into three major regions: the Mexican mainland, Baja Peninsula and samples of W. filifera. Third, for the Brahea palms, we partitioned all of the samples into three groups: Guadalupe Island, Cabo region and rest of the Baja Peninsula. Fourth, for both Washingtonia and Brahea palms, we tested the hypothesis that relict populations persisted within each of the sierras, which should be reflected in each sierra harboring a genetically distinctive population. Eight groups were specified for Washingtonia and ten for Brahea, each corresponding to a different sierra (For more details see Figure 2). AMOVA and genetic differentiation analyses were not carried out for the Brahea chloroplast data, as only three haplotypes were present and almost all of the individuals shared the same haplotype. The single B. elegans sample was also excluded from these analyses. For each AMOVA, statistical significance was determined using 10,000 permutations of the dataset.

Figure 2.

Figure 2

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Panel (a). Upper panel: maps of the Baja peninsula and continental Sonora showing sampled Washingotnia populations. Each of the maps represents one hypothetical divergence scenario tested within AMOVA. The a priori defined regions are separated by three hypothesized phylogeographical breaks, including: (1) current taxonomy, (2) three major geographic regions and (3) each sierra as unique genetic entity. Arrows indicate species or sierras as follows: SL, Sierra Laguna; SM, Sierra Mechudo; SG, Sierra la Giganta; SSP, Sierra San Pedro; SLI + SSF, combined Sierra Libertad and Sierra San Francisco; Cat, Cataviña; SJ, Sierra Juarez; and Son, Sierra Aguaje. Lower left panel: results of analysis of molecular variance (AMOVA) comparison of three vicariance scenarios, based on nuclear and plastid markers. Lower right panel: picture of one of the sampling sites of W. robusta in Sierra Mechudo (SM). Panel (b). Upper panel: maps of the Baja peninsula and Guadalupe Island showing sampled Brahea populations. Each of the maps represents one hypothetical divergence scenario tested with AMOVA. The a priori regions are separated by three hypothesized phylogeographical breaks, including (1) current taxonomy, (2) isolation of Cabo region after oceanic inundation of the Isthmus of La Paz, and (3) each sierra as unique genetic entity. Arrows indicate species or sierras as follows: SL, Sierra Laguna; SM, Sierra Mechudo; SSP, Sierra San Pedro; SSF, Sierra San Francisco; SLI, Sierra Libertad; SA, Sierra Asamblea; Cat, Cataviña; SSPM, Sierra San Pedro Martir; SJ, Sierra Juarez; and final tenth group GI, Guadalupe Island. Lower left panel: results of analysis of molecular variance (AMOVA) comparison of three vicariance scenarios, based on nuclear markers. Lower right panel: picture of one of the sampling sites of B. armata in Sierra Asamblea (SA)

Finally, we used a Bayesian approach to estimate the number of genetic clusters present within the data as implemented in BAPS 6 (Corander, Marttinen, Siren, & Tang, 2008; Corander, Siren, & Arjas, 2008; Corander, Waldmann, & Sillanpaa, 2003). For this analysis, individuals were first clustered without any previous knowledge of their sampling locations. This analysis was run using the mixture model to determine the most probable number of clusters (K) within the data. K was set from 1 to 10 and five replicates were performed for each value of K. An admixture analysis was then carried out with 50 reference individuals and 1,000 iterations. Finally, we spatially clustered the individuals using Voronoi tessellation and geo‐referenced sample location data. All of the spatial analyses were conducted separately for Washingtonia and Brahea.

2.4. Ecological niche modeling

To better understand the current and past population dynamics of Washingtonia and Brahea palms along the Baja Peninsula we performed Ecological Niche Modeling (ENM) using the maximum entropy method implemented in Maxent 3.4.0 (Phillips, 2017; Phillips, Anderson, & Schapire, 2006). Maxent attempts to estimate a probability distribution of species occurrence that is closest to uniform while still subject to environmental constraints (Elith et al., 2011). Information on the geographic distribution of Washingtonia and Brahea was based on a total of 49 and 44 unique presence records respectively. We combined our field data, information of natural occurrence of Washingtonia in the USA described in Cornett et al. (1986) and geo‐referenced occurrence data from www.gbif.org and www.bajaflora.org (Accessed March 2017). Each model included seven bioclimatic variables that we considered might have the strongest effect on the distribution of these species (mean temperature of wettest quarter, mean temperature of driest quarter, mean temperature of warmest quarter, mean temperature of coldest quarter, precipitation of wettest quarter, precipitation of driest quarter, and precipitation of coldest quarter). By restricting this analysis to a subset of the most promising variables, we avoided potential overfitting of the Maxent model (Peterson & Nakazawa, 2008). To gain a better perspective on temporal changes in the distributions of Washingotnia and Brahea palms, we predicted suitable climate envelopes for each genus using current ecological conditions (1960–1990) and the following three historical time periods: mid Holocene (~6,000 years BP), the last glacial maximum (~22,000 years BP) and the last interglacial (~130,000 years BP). All of the bioclimatic data were downloaded from WorldClim (www.worldclim.org) as a set of raster layers with a spatial resolution of 30 s (ca. 1 km) or in the case of the LGM data, 2.5 min (ca. 5 km) (Hijmans, Cameron, Parra, Jones, & Jarvis, 2005; Otto‐Bliesner, Marshall, Overpeck, Miller, & Hu, 2006; Watanabe et al., 2011). For each run, we used the default settings with 30 bootstrap replicates. The area under the receiver operating curve (AUC) was calculated to assess the model accuracy, with values between 0.7 and 0.9 indicating good discrimination (Swets, 1988). Jackknife analyses were performed to determine the relative contribution of each of environmental variable to the model of projected current distribution (Phillips, 2017).

In order to test the null hypothesis that the two Baja palm's species occupy identical climatic environments (“niches”), we performed a niche identity test using ENMtools 1.4.4 (Warren, Glor, & Turelli, 2010) with 1,000 pseudoreplicates. We then compared a distribution of niche similarities obtained from pairs of pseudoniches based on randomly sampled occurrence points with the actual niche overlap between Washingtonia and Brahea (Warren et al., 2010). The latter was quantified using Schoener's D (Schoener, 1968) and the standardized Hellinger distance (I) (Warren, Glor, & Turelli, 2008). Schoener's D assumes that the suitability scores are proportional to species abundance, whereas Hellinger's‐based I quantifies the probability distributions of two ecological niche models. Both similarity metrics range from 0 (no niche overlap) to 1 (identical niches) (Warren et al., 2010).

3. RESULTS

3.1. Molecular markers

We evaluated a total of ten chloroplast and nuclear loci that have been proposed for molecular studies of the Arecaceae (Bacon et al., 2008; CBOL Plant Working Group 2009; Jeanson et al., 2011). Of these, we selected five informative loci: matK, CISP 4, trnT‐trnD, trnG‐trnS, and trnF‐trnL for further analysis. The other loci either lacked sequence variation in a representative sample of individuals (rbcL and trnC‐rpoB), failed to PCR amplify (trnfM‐trnS) or amplified more than one PCR product (ITS2 and CISP 8).

3.2. Sequence diversity

The final data set included 2,294 bp of concatenated chloroplast sequence and 738 bp of concatenated nuclear sequence, from which all InDels had been removed (All DNA sequences newly generated in this study have been deposited in the GenBank database under Accession Numbers KY911112‐KY911153). In total, we obtained 89 nuclear and 81 plastid sequences for Washingtonia palms and 80 nuclear and 80 plastid sequences from Brahea palms, including a single sample of B. elegans from Mexican mainland (See Section 2 and Table 1 for more details). Pooling all of the samples, we obtained a total of 10 unique chloroplast and 19 nuclear haplotypes (Table 2, Figures 3 and 4). Levels of sequence diversity were generally low within the morphologically defined species, with individuals carrying either a single common haplotype or a handful of closely related haplotypes at low frequency (Table 2). As shown by the haplotype accumulation curves, our sample size was sufficiently large to encompass the majority of the genetic diversity present within the studied species (Figure S1).

Table 2.

Descriptive statistics for (a) chloroplast and (b) nuclear sequences isolated from five desert palm species

W. robusta W. filifera B. armata B. brandegeei B. edulis
(a) Chloroplast n samples 73 8 27 35 17
n haplotypes 5 2 1 2 1
Variable sites 4 1 – 6 –
h 0.53 0.43 – 0.51 –
π 0.0003 0.0002 – 0.001 –
(b) Nuclear n samples 82 7 27 38 14
n haplotypes 7 1 5 7 1
Variable sites 6 – 4 5 –
h 0.34 – 0.72 0.70 –
π 0.0006 – 0.0013 0.0014 –
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h haplotype diversity and π nucleotide diversity. We excluded B. elegans from these analyses as it was represented only by one sample.

Figure 3.

Figure 3

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Geographical distribution of Washingtonia and Brahea chloroplast haplotypes. Panel (a) shows a haplotype network in which the size of each pie chart is proportional to the number of individuals carrying the haplotype. Each tick mark on the solid lines indicates a single DNA mutation. The colors shown in the box correspond to species delineations based on morphological characters as described in Minnich et al. (2011). Geographical distributions of chloroplast haplotypes of (b) Washingtonia and (c) Brahea samples. Colors correspond to the different haplotypes

Figure 4.

Figure 4

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Geographical distribution of Washingtonia and Brahea nuclear haplotypes. Panel (a) shows a haplotype network in which the size of each pie chart is proportional to the number of individuals carrying the haplotype. Each tick mark on the solid lines indicates a single DNA mutation. The colors shown in the box correspond to species delineations based on morphological characters as described in Minnich et al. (2011). Geographical distributions of nuclear haplotypes of (b) Washingtonia and (c) Brahea samples. Colors correspond to the different haplotypes

3.3. Relationships among and within species

Parsimony networks were used to visualize relationships among the samples based on the concatenated chloroplast and nuclear sequences (Figures 3a and 4a respectively). As expected, Washingtonia and Brahea were deeply divergent from one another at both the chloroplast and nuclear DNA. Moreover, within the genus Washingtonia, W. robusta, and W. filifera differed by nine (chloroplast) and two (nuclear) fixed nucleotides and carried no shared haplotypes (Figures 3a and 4a). Accordingly, when we plotted the spatial distributions of the chloroplast and nuclear haplotypes, Washingtonia samples formed three distinct groups with no shared haplotypes among them (Figures 3b and 4b). These comprised a northern group of Washingtonia from the Sierra Juarez (SJ), a group from the Baja California Peninsula and a group of mainland populations.

Within the Brahea complex, contrasting results were obtained for the plastid and nuclear sequence data (Figures 3a,c and 4a,c). Despite extensive sampling and having sequenced over 2,000 bp of chloroplast DNA, all of the B. armata, B. edulis, and northern B. brandegeei samples were fixed for a single haplotype (Figure 3a,c) and thus could not be distinguished from one another. The single B. elegans sample that was collected from the Mexican mainland carried a unique chloroplast haplotype separated by five mutational steps from B. armata and B. edulis. B. brandegeei was represented by two haplotypes, one of which was shared with B. armata and B. edulis, whereas another haplotype was only found in samples from the SL population (Figure 3c). Correspondingly greater haplotype diversity was found at the nuclear sequence data, with a total of 11 haplotypes detected, although most of these were present at low frequencies. There was also considerably more haplotype sharing among the Brahea species, with only B. edulis being distinguished by a unique nuclear haplotype (Figure 4a). Spatial distributions of the nuclear haplotypes for Brahea did not reveal any clear geographical patterns along the Peninsula, but confirmed the uniqueness of Guadalupe Island palms (Figure 4c).

Pairwise differentiation statistics provided additional quantitative support for the patterns described above (Tables 3 and 4, Table S2). For example, within Washingtonia and for both the chloroplast and nuclear data, pairwise F st and Φst values were large and highly significant for the comparisons between W. filifera (SJ) and the peninsular and mainland W. robusta populations. In contrast, none of the comparisons among the sierras of the Baja Peninsula were significant (Table 3a,b).

Table 3.

Estimates of genetic differentiation among eight populations of Washingtonia. Pairwise F st and Φst values (above and below the diagonal respectively) are shown separately for (a) chloroplast and (b) nuclear genes

Sierra (Population) SJ Cat SLI + SSF SSP SG SM SL Son
(a) Chloroplast SJ – 0.97 *** 0.96 *** 0.98 ** 0.97 *** 0.97 *** 0.98 *** 0.97 ***
Cat 0.58 *** – −0.15 −0.13 −0.12 −0.13 −0.11 0.74 ***
SLI + SSF 0.46 ** −0.11 – −0.06 −0.08 −0.04 0.03 0.68 ***
SSP 0.69 ** −0.13 0.05 – 0.06 −0.02 −0.19 0.77 **
SG 0.54 *** −0.12 −0.09 0.06 – −0.04 0.08 0.72 ***
SM 0.61 *** −0.13 −0.03 −0.02 −0.04 – 0.00 0.74 ***
SL 0.71 *** −0.11 0.11 −0.19 0.08 0.00 – 0.79 ***
Son 0.61 *** 0.63 *** 0.51 *** 0.73 ** 0.58 *** 0.63 *** 0.74 *** –
(b) Nuclear SJ – 1.00 ** 1.00 *** 1.00 ** 0.91 *** 0.92 *** 0.85 *** 0.96 ***
Cat 1.00 ** – 0.00 0.00 −0.10 −0.11 −0.10 0.87 ***
SLI + SSF 1.00 ** 0.00 – 0.00 −0.06 −0.07 −0.06 0.89 ***
SSP 1.00 ** 0.00 0.00 – −0.13 −0.14 −0.14 0.86 **
SG 0.81 *** −0.06 −0.02 −0.10 – 0.01 0.00 0.76 ***
SM 0.89 *** −0.09 −0.06 −0.13 0.00 – −0.03 0.82 ***
SL 0.77 *** −0.05 −0.01 −0.09 −0.03 −0.01 – 0.72 ***
Son 0.87 *** 0.86 ** 0.87 *** 0.84 ** 0.72 *** 0.83 *** 0.71 *** –
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FDR corrected p‐values: *p < .05; **p < .01; ***p < .001, p‐values at α < 0.05 are highlighted in bold. The coding corresponds to the sampled sierras (See Section 2, Figure 1 and Table 1 for more details).

Table 4.

Estimates of genetic differentiation among the ten populations of Brahea based on the nuclear data. Pairwise F st and Φst values are shown above and below the diagonal, respectively

Sierra (Population) SJ SSPM Cat SA SLI SSF SSP SM SL GI
SJ – 0.78 * −0.09 0.41 0.29 0.61 * 0.55 * 0.66 ** 0.53 ** 0.97 ***
SSPM 0.78 * – 0.55 0.29 0.16 0.49 * 0.17 0.49 * 0.09 1 **
Cat −0.04 0.50 – 0.21 0.17 0.49 * 0.38 0.55 * 0.45 * 0.95 **
SA 0.27 0.50 −0.03 – −0.21 0.26 −0.14 0.42 * 0.16 0.94 **
SLI 0.30 0.37 0.04 −0.21 – 0.21 −0.11 0.31 * 0.09 0.86 ***
SSF 0.35 * 0.40 * 0.07 0.07 0.09 – 0.14 0.05 0.24 * 0.89 **
SSP 0.41 * 0.33 0.09 −0.17 −0.13 −0.00 – 0.25 −0.04 0.93 ***
SM 0.52 ** 0.56 * 0.30 0.30 0.28 * 0.01 0.15 – 0.16 0.92 ***
SL 0.48 ** 0.06 0.24 * 0.24 * 0.20 * 0.14 0.09 0.27 * – 0.88 ***
GI 0.90 *** 1 *** 0.81 *** 0.81 *** 0.71 *** 0.69 *** 0.77 *** 0.77 *** 0.71 *** –
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FDR corrected p‐values: *p < .05; **p < .01; ***p < .001, p‐values at α < 0.05 are highlighted in bold. The coding corresponds to the sampled sierras (See Section 2, Figure 1 and Table 1 for more details).

Within Brahea, we focused on the nuclear data, as only three chloroplast haplotypes were present, one of which was found in 78% of the samples. For the nuclear sequence data, Brahea samples were grouped into ten a priori defined geographical regions (See Section 2, Table 1 and Figures 1 and 2 for more details). The resulting F st and Φst values between Guadalupe Island and the other regions ranged from 0.69 to 1 and were thus highly significant (Table 4). We also detected significant differentiation between the southern (Cabo Region, Sierra del Mechudo, Sierra San Pedro) and northern (Sierra Juárez, Sierra Libertad and Cataviña) sierras (Table 4). After partitioning the samples based on taxonomically designated species, similarly high and significant F st and Φst values were obtained (Table S2).

Next, we used AMOVA to assess how sequence variation was partitioned among species and a priori defined geographical regions (Figure 2 and Table S3a,b). All partitioning schemes yielded significant estimates of among‐region differentiation. In the case of Washingtonia palms, of the three hypotheses that we tested, the grouping of the samples into three regions corresponding to W. robusta from the mainland, W. robusta from the Baja Peninsula and W. filifera yielded the largest among‐region variance components for nuclear (87%) and plastid (94%) data (Scenario 2 in Figure 2a). For Brahea palms, the proportion of variance attributable to differences among the ten sierras was greatest, at around 66% (Scenario 3 in Figure 2b), followed by among taxonomically designated species (62%) and B. brandegeei being restricted to SL (50%) (Table S4).

3.4. Bayesian cluster analysis

The above results were strongly supported by Bayesian cluster analyses of the combined chloroplast and nuclear sequence datasets conducted within BAPS. Without utilizing prior information on the sampling locations of individual palms, analysis of the chloroplast data revealed support for four genetic clusters (K = 4, Figure S2a). Two clusters were found within Washingtonia, corresponding to the taxonomically defined W. filifera and W. robusta. A further two clusters were found within Brahea, corresponding to B. brandegeei samples from the SL population plus the single sample of B. elegans from the mainland, and B. edulis plus all of the B. brandegeei samples north of the Cabo region and all of the B. armata individuals. Based on the nuclear data, only three clusters were identified (K = 3, Figure S2b). Specifically, all of the Washingtonia samples clustered together, as did all of the Brahea samples with the exception of B. edulis from Guadalupe Island, which formed a third cluster.

Finally, we used information on the sampling sites to conduct spatial clustering analyses within BAPS separately for Washingtonia and Brahea based on the chloroplast and nuclear data respectively (Figure 5). For Washingonia, Voronoi tessellation graphs of both the chloroplast (Figure 5a) and nuclear (Figure 5c) sequence data revealed two geographically separate genetic clusters, corresponding to W. filifera in the north (SJ) and W. robusta throughout the rest of the Baja Peninsula. Based on the nuclear data, an additional cluster was recovered corresponding to samples from the mainland Washingtonia populations (Figure 5c). For Brahea, the chloroplast data revealed three clusters (Figure 5b) that exactly mirror the spatial haplotype distributions shown in Figure 2c. By contrast, the nuclear data indicated the presence of only two genetic clusters (Figure 5d), one corresponding to the peninsular and mainland populations combined, and the second to Guadalupe Island.

Figure 5.

Figure 5

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Spatial clustering analysis of Washingtonia and Brahea samples using a Voronoi tessellation as implemented in BAPS. (a) Washingtonia spp. chloroplast data, (b) Brahea spp. chloroplast data, (c) Washingtonia spp. nuclear data, and (d) Brahea spp. nuclear data

3.5. Ecological niche modeling

AUC values of the ecological niche models of projected current distributions, averaged over 30 replicates, were around 0.97 for both Washingtonia and Brahea indicating good predictive model performance. For Washingtonia, the environmental variables that contributed the most to the Maxent model of projected current distribution were precipitation of the driest quarter, mean temperature of the coldest quarter and mean temperature of the wettest quarter in ascending order. Together these variables contributed over 70% of the explanatory power of the model, indicating that they are very good predictors of the contemporary geographical distribution of Washingtonia palms. For Brahea, precipitation of driest quarter, mean temperature of the warmest quarter and mean temperature of the driest quarter were the main predictors of geographical distribution, contributing over 67% of the explanatory power of the model (Table S5).

In general, the predicted distribution of Washingtonia under current conditions (Figure 6A) was similar to the actual distribution (Minnich et al., 2011 and Figure 1), with two major areas of high probability of occurrence, one in the southern Baja Peninsula (SL, SM and SG) and the other in the northern Baja Peninsula (SJ) and southern California. However, there were also some predicted areas where Washingtonia palms cannot currently be found, such as the Pacific coast around the 30th parallel north. The projected current distribution of Brahea was somewhat restricted in comparison to Washingtonia, with SL, SSP and SSPM being the main areas of high probability of occurrence (Figure 7a).

Figure 6.

Figure 6

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Probability of occurrence of Washingtonia palms on the Baja California: (a) at present; (b) during the mid Holocene; (c) during the last glacial maximum and (d) during the last interglacial. See the main text for more details

Figure 7.

Figure 7

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Probability of occurrence of Brahea palms on the Baja California: (a) at present; (b) during the mid Holocene; (c) during the last glacial maximum, and (d) during the last interglacial. See the main text for more details

During the mid Holocene (about 6,000 years ago) the predicted geographical distribution of Washingtonia was broader than the contemporary distribution, with favorable habitats situated especially along the Pacific coast of the central and southern Baja Peninsula (Figure 6b). By contrast, the predicted distribution of Brahea during the mid Holocene was similar to its current projected distribution (Figure 7b). Further back in time, during the last glacial maximum (about 22,000 years ago), both species appear to have been restricted largely to the southernmost tip of the peninsula, with Brahea also predicted to occur in a small area of the mid‐northern peninsula (Figures 6c and 7c). According to Maxent estimations, during the last interglacial (about 130,000 years ago), Washingtonia's predicted distribution shifted mainly to coastal areas of both the northern and southern peninsula (Figure 6d). Brahea on the other hand seems to had have experienced favorable conditions across much of the peninsula, which extended into SG, SSP and SSPM (Figure 7d). The estimated niche overlap for Washingtonia and Brahea was considerable of 0.55 and 0.7 using Schoener's D and Hellinger's‐based I, respectively. Nonetheless, randomization tests of niche identity indicated that Washingtonia and Brahea palms are not ecologically equivalent to each other (Figure S3), regardless of the measure of similarity used (Schoener's D or Hellinger's I).

4. DISCUSSION

We have generated baseline molecular data on species boundaries and the population structure of native palms of Baja California and Guadalupe Island, which provide new insights into the histories of these unique species. Our initial prediction regarding the levels of genetic diversity and phylogeography of Washingtonia and Brahea were only partially confirmed. In accordance with expectations, disjunct and isolated populations of Baja palms contained low haplotype diversity. Additionally, ecological barriers like sea channels appear to be responsible for high levels of isolation between groups on either side of the barrier. In contrast to expectation however, genetic structure and diversity distribution of Washingtonia and Brahea along the Peninsula were not the same. Detailed ecological niche modeling analysis provided an explanation for this trend, suggesting slightly different re‐colonization routes after the LGM and sensitivity to different ecological variables. Our work demonstrates the importance and advantages of a multispecies approach, as some relevant conclusions about each species can only be reached using a comparison among different, yet similar and related species.

4.1. Species delimitation

One of the main goals of our work was to establish species boundaries for Washingtonia and Brahea palms in the study area. The distribution of Washingtonia inferred from our sequence data is broadly in line with previously published morphological information (Felger & Joyal, 1999; Minnich et al., 2011). Despite alleged hybrids having been reported on the basis of morphological data at Cataviña (Cornett, 1987b) and hybridization between W. robusta and W. filifera being common under cultivation (Hodel, 2014), we found no shared haplotypes between W. robusta and W. filifera and the distributional limits of these two species inferred from the sequence data also did not overlap, the southern limit of W. filifera being Sierra Juarez and the northern limit of W. robusta being Cataviña (Figures 3 and 4). Overall, given the lack of shared haplotypes and strong sequence divergence between W. filifera and W. robusta, our data support the classification of these two taxa as separate, geographically delimited, species.

In contrast, our sequence data revealed mixed support for previous morphological species definitions within Brahea. For instance, Minnich et al. (2011) recently suggested that B. brandegeei is distributed on the southern part of the peninsula from the Sierra La Laguna to the Sierra San Francisco. However, this was not supported by either the nuclear or the chloroplast data, the former showing no obvious split in the genetic composition of Brahea populations along the entire length of the peninsula, while the latter revealed a lineage corresponding to B. brandegeei that appears to be restricted to the Cabo region (SL) of the Peninsula. Our study also included B. edulis samples from Guadalupe Island, allowing a comparison to be made with the peninsular Brahea populations. We found that B. edulis was strongly differentiated from the peninsular populations at the nuclear sequence data, being fixed for a unique haplotype, but that at the chloroplast sequence data B. edulis could not be distinguished from the northern peninsula populations corresponding to B. armata.

There are several possible explanations for the observed differences between the chloroplast and nuclear sequence data within Brahea. First, introgression of chloroplast DNA cannot be discounted, but this seems unlikely given the degree of geographic isolation of Guadalupe Island and its geological origin (Moran, 1996). Second, incomplete linage sorting of shared ancestral polymorphisms could be important, especially given the relatively low levels of observed sequence polymorphism, which could reflect slow chloroplast mutation rates in palms (Wilson, Gaut, & Clegg, 1990). Third, the chloroplast genome reflects seed‐mediated gene flow (Hamrick & Nason, 2000) suggesting that a contrasting pattern at the two types of marker could arise if partial geographical isolation interrupted seed‐mediated gene flow but not pollen‐mediated genetic exchange (Hamilton & Miller, 2002; Petit et al., 2005). Regardless of the exact explanation, incongruent phylogenetic signals between plastid and nuclear data are not uncommon in plants (Pillon et al., 2013), suggesting that an interesting avenue for further research in palms would be to develop a larger and more informative marker panels, for instance using new approaches such as genotyping by sequencing (Narum, Buerkle, Davey, Miller, & Hohenlohe, 2013).

4.2. Patterns of haplotype diversity and structure

Although we expected that sympatrically occurring Washingtonia and Brahea palms would exhibit similar patterns of haplotype structuring along the Baja Peninsula we found the opposite (Figures 3 and 4). For example, as inferred with AMOVA and BAPS, Washingtonia palms on the Baja Peninsula were clustered into two groups comprising palms from SJ and the rest of the peninsula. Contrastingly, AMOVA analysis of the nuclear sequences in Brahea favored a scenario in which each sierra was genetically distinct (Figure 2b, Scenario 3). These differences may be explained by the slightly distinct habitat requirements and differences in the drought and freezing tolerances of Washingtonia and Brahea (Cornett, 1987a,b; Franco‐Vizcaino et al., 2007; Minnich et al., 2011). In accordance, ENM indicated that although the strongest ecological predictor of the contemporary distribution of Washingtonia and Brahea palms was precipitation of driest quarter, the second most important variable affecting Washingtonia's distribution was the mean temperature of the coldest quarter, whereas for Brahea it was the mean temperature of the warmest quarter. Predicted temporal changes in the distribution of these two genera over the past 130,000 years also indicated that Washingotnia and Brahea probably responded differently to historical changes in climate (Figures 6 and 7). For example, the contemporary distribution of Washingtonia suggests that its range may have contracted over recent historical time whereas Brahea has maintained a similar distribution for at least 6,000 years.

Dispersal is an essential element that shapes patterns of genetic structure in the Arecaceae (Eiserhardt, Svenning, Kissling, & Balslev, 2011). Although many vertebrates like bats, coyotes and foxes have been proposed as possible seed dispersal agents for Washingtonia and Brahea, the effect of these agents on palm genetic diversity and structure has not been properly tested (Cornett, 2008; Wehncke et al., 2010). In the case of Brahea, it also appears that water pulses may be more significant in terms of seed dispersal than vertebrates (Wehncke et al. 2010; Wehncke, López‐Medellín, & Ezcurra, 2009). A comparative study that would quantify the differences in dispersal capacity between Washingtonia and Brahea would definitively help to further our understanding of this topic.

As expected, levels of haplotype diversity were low in Washingtonia for both the chloroplast and nuclear sequence data, whereas nuclear diversity in peninsular Brahea was somewhat higher (Figures 3 and 4). The levels of diversity that we found were broadly comparable to other relict plant species of the region (e.g., Guaiacum unijugum, McCauley et al., 2010; Quercus brandegeei, Cavender‐Bares et al., 2015) as well as to Washingtonia populations in the USA (McClenaghan & Beauchamp, 1986). Moreover, sequence diversity at the nuclear loci was not evenly distributed along the peninsula and also showed differences between Washingtonia and Brahea (Figure 4). In Washingtonia palms, higher diversity was found in the southern sierras (SL and SM), whereas in Brahea palms, the mid peninsular sierras (SSF and SLI) had the highest nuclear sequence diversity (Figure 4). Higher levels of diversity in the southern populations of Washingtonia may be explained by postglacial range expansion and re‐colonization of the northern peninsula from southern refugia, as has been suggested for other Baja Peninsula plant species (Clark‐Tapia & Molina‐Freaner, 2003; Gutiérrez Flores, García‐De León, León de la Luz, & Cota‐Sánchez, 2016; Nason, Hamrick, & Fleming, 2002). This scenario was also supported by ENM analysis (Figure 6c), which suggested that during the LGM, predicted suitable habitats for Washingtonia became restricted to a narrow coastal strip at the southern tip of the Baja Peninsula. Interestingly, another predicted habitat where Washingtonia was likely to survive was in southern California. Nonetheless, based on the observed haplotype distribution, palms from this refugium were able to re‐colonize only SJ and did not move further south. This may be explained by the observation that Sierra San Pedro Martir has acted as a natural dispersal barrier for Washingtonia (Minnich et al., 2011); ENM results also supported this explanation (Figure 6). However, W. robusta is naturally rare in the northern peninsula, has higher water requirements and seems to be less tolerant to low temperatures than Brahea (Minnich et al., 2011). We therefore cannot discount the possibility that these observed patterns could have been partly affected by selection favouring the retention of specific haplotypes through linkage disequilibrium to functional loci. One way to test for this would be to genotype functional genetic markers putatively involved in adaptation (Luikart, England, Tallmon, Jordan, & Taberlet, 2003).

The pattern of sequence diversity found in Brahea may be explained by the presence of refugia not in the south, but in the middle part of the peninsula (Garrick, Nason, Meadows, & Dyer, 2009). However, ENM analysis contradicted this explanation and showed that the predicted distribution of Brahea during the LGM was concentrated across relatively large areas in SL and SSPM (Figure 7). Another possibility that may explain the high genetic diversity of Brahea palms in the middle of the peninsula would be that this region represents the contact zone of recolonization between palms of the southern (SL) and northern (SSPM) refugia during the LGM. This hypothesis would also help to explain why it has been hard to established precise species boundaries between B. brandegeei from the southern and B. armata from the northern peninsula using morphological characteristics (Felger & Joyal, 1999; Minnich et al., 2011).

Moving to the Guadalupe Island palms, we found comparably much lower levels of chloroplast and nuclear diversity. Only one chloroplast and one nuclear haplotype was recovered for 17 and 14 B. edulis individuals respectively. This pattern is in contrast to results found for other tree species of the Island (e.g., Pinus radiata, Karhu, Vogl, Moran, Bell, and Savolainen (2005) and Cupressus guadalupensis, Rosas‐Escobar et al. (2011). Although founder effects are often invoked to explain low levels of genetic variation, many other factors may influence the genetic diversity of endemic island plants, including extrinsic ones like island size, distance to the mainland and the amount of available habitat. Another group of factors comprise intrinsic properties such as mutation rate, dispersal capacity, diversity of the population of provenance, and the capacity to respond to human disturbance (Stuessy, Takayama, Lopez‐Sepulveda, & Crawford, 2014). When all of these factors are taken into account, the low genetic diversity detected for B. edulis is not surprising. For example, although the total area of Guadalupe Island is about 240.00 km2, B. edulis occupies only 0.8 km2 at the foggy northern extreme of the Island (Garcillán et al., 2012; Oberbauer, 2005). This restricted available habitat reduces the potential establishment of new populations and limits effective population size (Frankham, 1996). Another important factor that may explain the low diversity of B. edulis is the low diversity of Brahea populations from the Baja Peninsula. For example, only two chloroplast haplotypes were detected in over 60 peninsular Brahea individuals. Additionally, the long generation time of Brahea (Bullock & Heath, 2006) and low mutation rates in the Arecaceae (Wilson et al., 1990) may both limit the rate at which new genetic variation is acquired by B. edulis (Stuessy et al., 2014).

4.3. Congruence with historical scenarios

During the last six million years, the Baja California Peninsula has undergone many geological changes that have profoundly affected the distribution and genetic structure of plant and animals species (Dolby et al., 2015; Riddle et al., 2000). Most notably, the formation of the Gulf of California and separation of the Baja California Peninsula from the Mexican mainland, which began approximately 6 million years ago, resulted in the complete or partial isolation of many plant and animal populations on either side of the break (Dolby et al., 2015; Garrick et al., 2009; Gutiérrez Flores et al., 2016; Riddle et al., 2000). Currently, the Gulf of California represents a major barrier to gene flow even for certain organisms with moderate dispersal capabilities (Grismer, 2000; Riddle et al., 2000), so in some respects it is unsurprising that it also appears to impeded gene flow in sessile organisms like plants (Cavender‐Bares et al., 2015). Consistent with this, we found a strong pattern of haplotype differentiation between mainland and peninsular W. robusta at both nuclear and chloroplast sequences. Our results from the chloroplast data for Brahea were similar, but as only one individual from the Mexican mainland was analyzed, we could not draw any firm conclusions. Nonetheless, although we lacked samples from the Mexican mainland for Brahea, we were able to include an endemic Brahea palm species from Guadalupe Island. This volcanic island has never been in contact with the Baja Peninsula and as a consequence almost 16% of its native plant species are endemics (Batiza, 1977; León De La Luz et al., 2003). Deep nuclear isolation of Guadalupe Island's Brahea from its peninsular sister species is consistent with a strong effect of dispersal barriers like sea channels on the population structure of Brahea palms (Karhu et al., 2005; Rosas‐Escobar et al., 2011).

Historically, the Baja has also undergone a series of submersions and uplifts (Lindell et al., 2006; Riddle et al., 2000). During these partial submersions, the Peninsula was fragmented into one or more islands and the Pacific Ocean was connected to the Gulf of California. More specifically, inundation of the Isthmus of La Paz isolated the Cabo region (SL) from the rest of the Baja Peninsula, whereas the mid‐peninsular seaway temporally isolated the southern and northern parts of the Baja Peninsula (Lindell et al., 2006; Riddle et al., 2000). Nonetheless, the exact locations of the proposed seaways as well as the timing of their formation are still under debate (Dolby et al., 2015). Regardless of the precise time and location estimates, these breaks are thought to be responsible for the observed patterns of genetic structuring in a variety of taxa (Garrick et al., 2009; Lindell, Méndez de la Cruz, & Murphy, 2005; Lira‐Noriega, Toro‐Núñez, Oaks, & Mort, 2015; Riddle et al., 2000; Upton & Murphy, 1997), although alternative explanations have also been proposed (Gutiérrez Flores et al., 2016). Washingtonia's nuclear and plastid sequence data did not provide any support for either of these breaks, with clustering results indicating the presence of a single genetically homogeneous population along the peninsula. By contrast, for Brahea, the chloroplast data strongly supported the presence of two genetically differentiated clades along the peninsula (Figures 3a,c, and 5b), providing support for historical marine intrusion into lowland areas of the Isthmus of La Paz.

CONFLICT OF INTEREST

None declared.

Supporting information

 

Click here for additional data file. (482.9KB, docx)

ACKNOWLEDGMENTS

The authors are thankful to Alfonso Medel Narváez, Raymundo Domínguez Cadena and Julio Montoya for participating in the collection of samples. Logistic support for collecting on Guadalupe Island and Sierra La Libertad were provided by the Grupo de Ecología y Conservación de Islas and Victor Sanchez Sotomayor, respectively. The work was funded by project Red Temática de Investigación of CONACyT (280030) and CONACYT Basic Science project (251919). We acknowledge the financial support of the German Research Foundation (DFG) and the Open Access Publication Fund of Bielefeld University for the article processing charge. We are also thankful to Drs. Eduardo Vivas, Patricia Galina and Pedro Peña Garcillán for providing helpful comments.

Klimova A, Hoffman JI, Gutierrez‐Rivera JN, Leon de la Luz J, Ortega‐Rubio A. Molecular genetic analysis of two native desert palm genera, Washingtonia and Brahea, from the Baja California Peninsula and Guadalupe Island. Ecol Evol. 2017;7:4919–4935. https://doi.org/10.1002/ece3.3036

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