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Phylogenomic insights into the diversification of in the Isthmura bellii group across the Mexican highlands

Article in Molecular Phylogenetics and Evolution · March 2018 DOI: 10.1016/j.ympev.2018.03.024

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Molecular Phylogenetics and Evolution

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Phylogenomic insights into the diversification of salamanders in the T Isthmura bellii group across the Mexican highlands ⁎ Robert W. Bryson Jr.a,b, , Eugenia Zarzab,c, Jared A. Grummerd, Gabriela Parra-Oleae, Oscar Flores-Villelaf, John Klickaa, John E. McCormackb a Department of Biology & Burke Museum of Natural History and Culture, University of Washington, Seattle, WA, USA b Moore Laboratory of Zoology, Occidental College, Los Angeles, CA, USA c Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Irapuato, Guanajuato, Mexico d Department of Zoology, Biodiversity Research Centre and Beaty Biodiversity Museum, University of British Columbia, Vancouver, Canada e Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad de México, Mexico f Museo de Zoología, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México, Mexico

ARTICLE INFO ABSTRACT

Keywords: Mountain formation in Mexico has played an important role in the diversification of many Mexican taxa. The Biogeography Trans-Mexican Volcanic Belt in particular has served as both a cradle of diversification and conduit for dispersal. Genomics We investigated the evolutionary history of the Isthmura bellii group of salamanders, a widespread Mexico across the Mexican highlands, using sequence capture of ultraconserved elements. Results suggest that the I. bellii Phylogeography group probably originated in southeastern Mexico in the late Miocene and later dispersed across the Trans- Mexican Volcanic Belt and into the Sierra Madre Occidental. Pre-Pleistocene uplift of the Trans-Volcanic Belt Ultraconserved elements fi fi Sequence capture likely promoted early diversi cation by serving as a mesic land-bridge across central Mexico. These ndings highlight the importance of the Trans-Volcanic Belt in generating Mexico’s rich biodiversity.

1. Introduction Occidental (I. sierraoccidentalis). The nominate species, I. bellii, is widely distributed across the Trans-Mexican Volcanic Belt, southern Sierra Mexico ranks fifth in the world in amphibian diversity (Flores- Madre Oriental, western Sierra Madre del Sur, and Central Mexican Villela, 1993; Parra-Olea et al., 2014), and over half of all amphibian Plateau. Salamanders in the I. bellii group are exclusively terrestrial and species in Mexico are endemic (Parra-Olea et al., 2014). The complex found in humid microenvironments within a variety of forested habi- evolution of Mexico’s landscape since the Miocene has stimulated ex- tats. Isthmura bellii, I. boneti, I. corrugata, I. gigantea, I. naucampatepetl, tensive diversification and linked Neotropical and Nearctic biotas. and I. sierraoccidentalis are most frequently found in mixed pine-oak Mountain formation in particular has heavily impacted diversification forest, but also inhabit oak, cloud, and fir forests. Isthmura maxima is of Mexican taxa (Mulcahy et al., 2006; Rovito et al., 2015, 2012; found at lower elevations within the Sierra Madre del Sur in tropical Streicher et al., 2014) and relatively young mountains such as the semi-deciduous forest. Trans-Mexican Volcanic Belt have served as both a cradle of diversifi- The phylogeny of the I. bellii group has been studied using mi- cation and conduit for dispersal (Parra-Olea et al., 2012; Rovito et al., tochondrial DNA (Parra-Olea et al., 2005; Sandoval-Comte et al., 2017). 2015, 2013). Although this single-gene approach can reveal valuable information The Isthmura bellii group of salamanders is comprised of seven about evolutionary history (e.g., Zink and Barrowclough, 2008; Bryson species distributed across the major mountainous regions of Mexico et al., 2014), stochastic events such as sex-biased dispersal and adaptive (Fig. 1; Parra-Olea et al., 2005; Sandoval-Comte et al., 2017). Six spe- selection can mislead phylogenetic inference based on only the mi- cies have small distributions, including two restricted to the eastern tochondrial genome (Ballard and Whitlock, 2004; Toews and Brelsford, Sierra Madre del Sur (I. boneti and I. maxima), three found in the 2012). Recent advances in DNA sequencing have enabled researchers to southern Sierra Madre Oriental and easternmost region of the Trans- assay massive amounts of genetic data collected from across the Mexican Volcanic Belt (I. corrugata, I. gigantea and I. naucampatepetl), genome. Here we utilize sequence capture of ultraconserved elements and one known only from a small region of the northern Sierra Madre (UCEs) to study the phylogeography of salamanders in the I. bellii

⁎ Corresponding author at: Department of Biology & Burke Museum of Natural History and Culture, University of Washington, Seattle, WA, USA. E-mail address: [email protected] (R.W. Bryson). https://doi.org/10.1016/j.ympev.2018.03.024 Received 1 October 2017; Received in revised form 10 February 2018; Accepted 15 March 2018 Available online 16 March 2018 1055-7903/ © 2018 Elsevier Inc. All rights reserved. R.W. Bryson et al. Molecular Phylogenetics and Evolution 125 (2018) 78–84

Fig. 1. Localities of salamanders in the Isthmura bellii group sampled for this study. Major mountainous regions of Mexico are labeled. group. Ultraconserved elements are a class of highly conserved and 2.2. Sequence capture and next-generation sequencing abundant nuclear loci scattered throughout the genome (Faircloth et al., 2012), and together with DNA adjacent to UCE locations, are We extracted genomic DNA from tissue using a Qiagen (Valencia, emerging as an important genomic marker set for phylogeographic CA) DNeasy Blood and Tissue extraction kit. We visualized extractions studies (McCormack et al., 2016; Newman and Austin, 2016; Smith on an agarose gel to ensure that fragments were > 200 bp and quanti- et al., 2014; Zarza et al., 2016). We generate a UCE data set from fied the resulting double-stranded DNA using a Qubit 2.0 Fluorometer samples collected across the range of the I. bellii group to estimate a (Carlsbad, CA). To collect genomic data, we followed the protocol for time-calibrated phylogeny. We then infer the geographic origin and UCE library preparation and enrichment from Faircloth (2012, 2013a). dispersal of the group across the Mexican highlands using Bayesian We sheared 100 ng of genomic DNA per sample at a 20 ng/µl con- phylogeographic modeling. Results will provide phylogenomic insights centration to a size distribution peak of ∼400–600 bp using a Bioruptor into the diversification of an endemic amphibian that is widely dis- Ultrasonicator (Diagenode). We prepared genomic libraries for each tributed across the Mexican highlands. sheared sample with a KAPA LTP library preparation kit for the Illu- mina platform, attaching custom indexing tags (Glenn et al., 2016)to DNA fragments from each sample to allow multiplexing during the 2. Methods capture phase. We enriched pools for 5060 UCE loci using a set of synthetic RNA probes (MYbaits_Tetrapods-UCE-5K kit, Mycroarray) 2.1. Sampling following the standard UCE enrichment protocol (Faircloth et al., 2012), but with a slight modification. Amphibian genomes have large We sampled 48 salamanders in the I. bellii group (Fig. 1, Table S1), and variable genome sizes with a great percentage of repetitive DNA including 5 of the 7 currently recognized species (Parra-Olea et al., (Olmo, 1991). We wanted to decrease the potential risk of probes hy- 2005; Rovito et al., 2015). We were unable to obtain samples of I. bridizing to repetitive elements, which might reduce the efficiency of corrugata and I. naucampatepetl, two rare species endemic to small re- the enrichment (McCartney-Melstad et al., 2016). Previous attempts to gions of central Veracruz (Parra-Olea et al., 2008; Sandoval-Comte optimize sequence capture in salamanders suggested that increasing et al., 2017). Sampling was focused on the wide-ranging species I. bellii. both the amount of individual DNA in the hybridization reaction and We included two samples of Aquiloeurycea cephalica and one Pseu- the concentration of the Cot-1 blocker reduced the rates of PCR du- doeurycea unguidentis as outgroups (Rovito et al., 2015). plicates, improving the efficiency of sequence capture (McCartney- Melstad et al., 2016). Thus, we modified the Faircloth (2012)

79 R.W. Bryson et al. Molecular Phylogenetics and Evolution 125 (2018) 78–84 enrichment protocol accordingly. We increased the amount of the Cot- ancestral locations by utilizing a Bayesian posterior tree distribution; chicken blocker in the reaction up to 12×. Additionally, we included visualization of this uncertainty is in the form of geographic credibility only 6 individuals per pool (instead of 8) to increase the amount of DNA intervals (in our analyses, 80% of the high posterior density) at any per individual in the reaction to 83 ng. After enrichment and recovery point in time (Lemey et al., 2010). We used the full dataset to infer the PCR, we verified that library size range was between 400 and 600 bp ancestral location of the I. bellii group, but later pruned outgroups from using a Bioanalyzer. We quantified the enriched pools using qPCR and the tree for visualization purposes. We used the gamma RRW model for combined them in equimolar ratios. The samples were sequenced on an the geographic diffusion model prior and a jitter window size of 0.5. We Illumina HiSeq 2500 at The HudsonAlpha Genome Sequencing Center ran analyses for 40 million generations, sampling every 1000 genera- with a 125 bp paired-end sequencing. tions, using the same BEAST priors specified above. The run was re- peated from a different starting seed to verify consistency between runs. 2.3. Bioinformatics We generated a maximum clade credibility tree using TreeAnnotator which was then input in SPREAD v.1.0.5 (Bielejec et al., 2011) to vi- After sequencing, we followed the standard PHYLUCE v.1.5.0 pi- sualize phylogeographical reconstructions at 6.25, 4.25, 2.25, and 0 Ma peline for processing target-enriched UCE data (Faircloth, 2016). As using the “TimeSlice” feature. These time slices were displayed in part of this pipeline, we trimmed reads of adapter contamination and Google Earth v.6.0.1 (Google Inc.) using the keyhole-markup language low-quality bases with Illumiprocessor (Faircloth, 2013b) and Trim- (kml) format. momatic (Bolger et al., 2014). We then assembled cleaned reads into contigs using Trinity (Grabherr et al., 2011), and aligned assembled 3. Results contigs to the original UCE probe sequences. We created a taxon set fi containing all samples, and used this taxon set to make a FASTA le 3.1. Genetic data containing all data for all taxa. We used MAFFT (Katoh and Standley, 2013) to then create alignments across all loci. After examining the We captured an average of 1045 UCE loci per sample fi number of UCE loci captured per sample, we created a nal con- (range = 361–1461; Table S1), excluding five samples that contained catenated data matrix with up to 50% missing data per locus (meaning fewer than 25 loci each (Table S1) that were removed before final each locus contained data for 50% or more of the total number of in- alignments. Loci were on average 349 bp in length dividuals). Increasing the proportion of missing data from 30% to 50% (range = 233–2777 bp) and each locus had an average of 5.7 parsi- fi resulted in 298 more loci in the nal dataset, and previous studies have mony-informative sites (range = 0–41). The final dataset contained shown that analyses of concatenated phylogenomic data (see below) 1094 loci and was 381,442 bp in length. Data matrices were deposited are generally robust to large amounts of missing data (Burleigh et al., in Dryad (https://doi.org/10.5061/dryad.875j1k8). 2015; Hosner et al., 2016).

2.4. Time-calibrated phylogenetic estimation 3.2. Time-calibrated phylogenetic estimation

We estimated a time-calibrated phylogeny using BEAST v.1.8.2 Our phylogenetic analyses of the concatenated dataset revealed a (Drummond et al., 2012). We used a GTR + G model of sequence history of pre-Pleistocene divergences among most species in the I. bellii evolution, an uncorrelated lognormal relaxed clock, and a Yule process group and strong phylogeographic structure within I. bellii (Fig. 2). tree prior, and ran analyses for 40 million generations, retaining trees Isthmura boneti and I. maxima from the eastern Sierra Madre del Sur and parameters every 10,000 steps. Results were visualized in Tracer formed a clade that diverged from the rest of the group at around 6 Ma v.1.6 (Rambaut and Drummond, 2007) to confirm acceptable mixing (see Fig. S1 for mean estimated dates and 95% error bars). Samples of I. and likelihood stationarity, appropriate burn-in, and effective sample gigantea from the southern Sierra Madre Oriental formed a clade, which sizes above 200 for all estimated parameters. Parameters associated split from a large clade of the last two species in the group (I. bellii + I. with the lognormal relaxed clock model failed to converge during sierraoccidentalis) about 5 Ma. Samples of I. bellii grouped together in preliminary runs, so we ran final analyses using a strict clock model, three main geographically structured clades corresponding to portions which produced similar trees and mean estimated divergence dates of the Sierra Madre Oriental in San Luis Potosí, Querétaro, and Hidalgo ‘ ’ across replicate runs. We discarded the first 25% of trees as burnin and ( Sierra Madre Oriental clade), parts of the western Sierra Madre del ‘ ’ summarized the maximum clade credibility tree with median heights Sur in Guerrero ( Sierra Madre del Sur clade), and a large region across using TreeAnnotator v.1.8.2 (Drummond et al., 2012). The analysis was the Trans-Mexican Volcanic Belt, Central Mexican Plateau, and Sierra ‘ ’ repeated twice from different starting seeds to confirm adequate mixing Madre Occidental ( western Mexico clade). Isthmura sierraoccidentalis and consistent results. grouped within the western Mexico clade, which also contained addi- To time-calibrate our phylogeny, we used two calibration points tional phylogeographic structure. Divergences among these three geo- based on results of a previous biogeographic study of Neotropical ple- graphic clades occurred in succession between 4 and 4.5 Ma during the thodontid salamanders (Rovito et al., 2015). We calibrated the split Pliocene. between Pseudoeurycea (represented in our study by P. unguidentis) and the clade of Isthmura + Aquiloeurycea using a normal prior with a mean 3.3. Bayesian phylogeography of 23 million years ago (Ma) and standard deviation of 2.5 Ma, resulting in a 95% highest probability density (HPD) ranging from 19 to 27 Ma. Results suggested the I. bellii group originated in southeastern The divergence of Isthmura and Aquiloeurycea was calibrated using a Mexico along the mountainous region encompassing the southern end normal prior with a mean of 15 Ma and a standard deviation of 1.2 Ma, of the Sierra Madre Oriental, eastern edge of the Trans-Mexican creating a 95% HPD ranging from 13 to 17 Ma. Volcanic Belt, and Sierra Madre del Sur of Oaxaca (Fig. 3a). By around 4.25 Ma, the group had begun to spread west across the central Trans- 2.5. Bayesian phylogeography Mexican Volcanic Belt (Fig. 3b). This western expansion continued over the next several million years, and by the start of the Pleistocene, the We inferred the geographic origin and spatial diffusion of sala- group was distributed across most of the Trans-Mexican Volcanic Belt manders in the I. bellii group using a continuous relaxed random walk and the southern Sierra Madre Occidental (Fig. 3c). Within the last two (RRW) diffusion model (Lemey et al., 2010, 2009) in BEAST. This million years, the group colonized the northern Sierra Madre Occi- model incorporates phylogenetic uncertainty when reconstructing dental (Fig. 3d).

80 R.W. Bryson et al. Molecular Phylogenetics and Evolution 125 (2018) 78–84

Fig. 2. Time-calibrated phylogeny of salamanders in the Isthmura bellii group inferred from concatenated UCE loci. The three major geographic clades of I. bellii are delineated. Mean estimated divergence dates and 95% highest posterior densities are given in Fig. S1. Nodes throughout the tree were supported by ≥0.95 posterior probability; the single exception is labeled with the posterior probability value.

4. Discussion group. For example, I. corrugata and I. naucampatepetl are restricted to the eastern edge of the Trans-Mexican Volcanic Belt, I. gigantea occurs 4.1. Phylogeography of the I. bellii group to the north, populations of I. bellii are found just west of this region, and I. boneti is distributed directly to the south. Like many Neotropical salamanders, the I. bellii group appears to Following early diversification, the Trans-Mexican Volcanic Belt have originated in southeastern Mexico (Fig. 3; Rovito et al., 2015). may have served as a mesic high-elevation land bridge that allowed the This geographically complex region of Mexico harbors an incredibly I. bellii group to disperse into western Mexico. Most of this volcanic diverse assemblage of endemic (Parra-Olea et al., 2014). chain of mountains was created before the onset of the Pleistocene Divergences among most of the currently described species in the I. (Ferrari et al., 2000, 1999; Gómez-Tuena et al., 2007). Results from our bellii group occurred during the late Miocene and Pliocene (Fig. 2). The Bayesian phylogeographic modeling suggest that members of the I. bellii timing and location of these early divergences suggest that pre-Pleis- group probably dispersed across the Trans-Mexican Volcanic Belt and tocene uplift of the Trans-Mexican Volcanic Belt (Gómez-Tuena et al., into the southern Sierra Madre Occidental between 4 and 2 Ma (Fig. 3). 2007) may have promoted diversification. The formation of this range At the start of the Pleistocene, the I. bellii group likely had a fragmented has had a strong impact on genetic structure of codistributed sala- distribution much like that seen today (Parra-Olea et al., 2005). Once manders (Hime et al., 2016; Parra-Olea et al., 2012; Rovito et al., 2013; reaching the highlands of the Sierra Madre Occidental, the group spread Velo-Antón et al., 2013) and other amphibians (Bryson et al., 2014; northward during the Pleistocene and eventually colonized the Mulcahy et al., 2006; Zarza et al., 2017). Uplift of the Trans-Mexican northern Sierra Madre Occidental. The large distributional gap ob- Volcanic Belt in eastern Mexico may have subdivided a previously served today between I. sierraoccidentalis in the northern Sierra Madre contiguous Sierra Madre Oriental (Corona et al., 2007; Ferro et al., Occidental and populations of I. bellii in the southern part of this range 2017), and the complex topography and sharp environmental gradients (Fig. 1) may have been caused by the warmer, drier climate that that developed in this region may have isolated taxa in the I. bellii marked the end of the Pleistocene and subsequent Holocene

81 R.W. Bryson et al. Molecular Phylogenetics and Evolution 125 (2018) 78–84

Fig. 3. Reconstructions of the spatial history of salamanders in the Isthmura bellii group across four time slices. Polygons represent 80% highest posterior density intervals for the spatial location of ancestral populations. fragmentation of Madrean pine-oak woodlands (Metcalfe et al., 2000). sentiments based on mtDNA and allozymes (Parra-Olea et al., 2005). It is also possible that future field work along the relatively rugged and Now that several lines of evidence (genetic data and geography) are remote intervening region will turn up new undocumented populations converging, the taxonomy of these salamanders needs to be re- that will fill in the gap. evaluated. Phylogenetic relationships among species in the I. bellii group in- The two samples of I. sierraoccidentalis included in our study are ferred in this study are generally congruent with results based on clustered within I. bellii, similar to results based on mtDNA (Parra-Olea mtDNA (Parra-Olea et al., 2005; Sandoval-Comte et al., 2017). Isthmura et al., 2005). This former subspecies of I. bellii was recently elevated to boneti and I. maxima are sister species, I. gigantea is sister to a clade full species based on differences in ecology, distribution, and coloration comprised of I. bellii + I. sierraoccidentalis, and I. sierraoccidentalis is (Rovito et al., 2015). Although the apparent geographic isolation and embedded within I. bellii. Parra-Olea et al. (2005) found that mi- unique coloration of I. sierraoccidentalis argue for species recognition, tochondrial pairwise divergences among species ranged from 5 to 15% recognizing it as such renders I. bellii paraphyletic, based on current (based on cytochrome b). If a generalized 2% rate of mitochondrial taxonomy. Given the phylogeographic structure observed within the evolution between lineages is applied (Brown et al., 1979), then di- wide-ranging species I. bellii (Fig. 2), one solution would be to divide I. vergences among species would have occured around 2.5–7.5 Ma, bellii into finer taxonomic units, a consideration proposed in previous predating the Pleistocene. Mitochondrial pairwise divergences within research (Parra-Olea et al., 2005). Alternatively, I. sierraoccidentalis species ranged up to 8.9%, and among I. bellii localities also represented could be subsumed within a single wide-ranging species, I. bellii, al- in our study, ranged from 6.7% (between samples from Guerrero and though doing so would effectively discount the suite of differences Jalisco) to 0% (between samples from near Cd. Guzmán, Jalisco), based described in Rovito et al. (2015). Such decisions await a detailed ex- on trimmed cytochrome b sequences (GenBank accession numbers amination of museum specimens representing each of the geographic AF451194, AY864686–87, AY864689–92) analyzed with MEGA6 clades and additional genetic data to estimate potential gene flow (Tamura et al., 2013). The estimated divergence between I. bellii from among clades. Guerrero and Jalisco would be around 3.4 Ma if using a 2% clock rate, Our results highlight two possible examples of sympatry of I. bellii similar to our estimated date of 3.9 Ma between I. bellii from Guerrero group species, or alternatively, reveal erroneous identifications re- and I. bellii from western Mexico (Fig. 2). However, we estimated that ported in the literature. The salamanders we sequenced from samples from near Cd. Guzmán, Jalisco (MXH141-144) diverged from Tepehuacan de Guerrero in Hidalgo were genetically similar to geo- each other at around 2.2 Ma (Fig. 2). Given that these samples were graphically adjacent I. bellii (Fig. 2). Badillo-Saldaña et al. (2015) re- collected from within 1 km of each other, this finding casts doubt on ported I. gigantea occurring in this same area. Similarly, our samples intrapopulation divergences inferred in our study. This may be an ar- from near Malinaltepec in eastern Guerrero were genetically similar to tifact of the large number of unique mutations within individual sam- samples of I. bellii from farther west in Guerrero (Fig. 2). García- ples based on the sheer size of our dataset (hundreds of thousands of bp Vázquez and Durán-Fuentes (2012) and Palacios-Aguilar et al. (2016) of sequence data per individual) or some unknown cause. Regardless, reported new records of I. maxima from this same region of Mal- we caution against overinterpreting intrapopulation divergence dates inaltepec. More research is needed on salamanders from these areas to among I. bellii group samples in our study. verify which scenario is correct—sympatry or specimen mis- identifications—to aid conservation efforts for this group of charismatic salamanders (Lips et al., 2005; Rovito et al., 2015; Wilson et al., 2013). 4.2. Taxonomic implications

Our results based on phylogenetic analyses of over 350,000 bp of 5. Conclusion genomic data provide additional evidence that the wide-ranging species I. bellii may be comprised of several cryptic species, echoing previous Sequence capture of UCEs appears to be a promising method for

82 R.W. Bryson et al. Molecular Phylogenetics and Evolution 125 (2018) 78–84 studying the phylogeography of salamanders, consistent with findings multiple evolutionary timescales. Syst. Biol. 61, 717–726. http://dx.doi.org/10. in a recent study of Plethodon salamanders (Newman and Austin, 2016). 1093/sysbio/sys004. Ferrari, L., Conticelli, S., Vaggelli, G., Petrone, C.M., Manetti, P., 2000. Late Miocene Our results using UCE sequence data suggest that the I. bellii group volcanism and intra-arc tectonics during the early development of the Trans-Mexican probably originated in southeastern Mexico in the late Miocene and Volcanic Belt. Tectonophysics 318, 161–185. http://dx.doi.org/10.1016/S0040- subsequently dispersed across the Trans-Mexican Volcanic Belt and into 1951(99)00310-8. Ferrari, L., López-Martínez, M., Aguirre-Díaz, G., Carrasco-Núñez, G., 1999. Space-time the Sierra Madre Occidental. The formation of the Trans-Volcanic Belt patterns of Cenozoic arc volcanism in central Mexico: From the Sierra Madre may have promoted early diversification in the group, and later served Occidental to the Mexican Volcanic Belt. Geology 27, 303–306. as a mesic conduit to allow dispersal into western Mexico, highlighting Ferro, I., Navarro-Sigüenza, A.G., Morrone, J.J., 2017. Biogeographical transitions in the the importance of this mountain range in generating Mexico’s rich Sierra Madre Oriental, Mexico, shown by chorological and evolutionary biogeo- graphical affinities of passerine birds (Aves: Passeriformes). J. Biogeogr. 44, biodiversity. 2145–2160. http://dx.doi.org/10.1111/jbi.13015. Flores-Villela, O., 1993. Herpetofauna of Mexico: Distribution and endemism. In: Acknowledgments Ramamoorthy, T.P., Bye, R., Lot, A., Fa, J. (Eds.), Biological Diversity of Mexico: Origins and Distribution. Oxford University Press, New York, pp. 253–280. García-Vázquez, U.O., Durán-Fuentes, I., 2012. Geographic distribution: Pseudoeurycea We thank the following curators and institutions for providing tissue maxima. Herpetol. Rev. 43, 438. ff samples: Ambrose Monell Cryo Collection and D.R. Frost (AMNH), D. Glenn, T.C., Nilsen, R., Kieran, T.J., Finger, J.W., Pierson, T.W., Bentley, K.E., Ho berg, S., Louha, S., Garcia-De-Leon, F.J., Portilla, M.A. del R., Reed, K., Anderson, J.L., Wake and C. Spencer (MVZ), and J.A. Campbell and C. Franklin (UTA). Meece, J.K., Aggery, S., Rekaya, R., Alabady, M., Belanger, M., Winker, K., Faircloth, We thank the numerous people who assisted in the field, including U.O. B.C., 2016. Adapterama I: Universal stubs and primers for thousands of dual-indexed Garcia-Vazquez, J. Jones, F. R. Mendoza-Paz, the late F. Mendoza- Illumina libraries (iTru & iNext). bioRxiv 049114. doi:10.1101/049114. Gómez-Tuena, A., Orozco-Esquivel, M.T., Ferrari, L., 2007. Igneous petrogenesis of the Quijano and G. Quijano-Manila, S. Rovito, B.T. Smith, I. Solano- Trans-Mexican Volcanic Belt, in: Special Paper 422: Geology of México: Celebrating Zavaleta, and M. Torocco. This project was funded in part through the Centenary of the Geological Society of México. Geological Society of America, pp. grants from the American Museum of Natural History (Theodore 129–181. doi:10.1130/2007.2422(05) Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., Adiconis, Roosevelt Memorial Fund), Southwestern Association of Naturalists X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, (Howard McCarley Student Research Award), UNAM (PAPIIT 224009), A., Rhind, N., di Palma, F., Birren, B.W., Nusbaum, C., Lindblad-Toh, K., Friedman, UNLV (Graduate and Professional Student Association), and NSF (DEB- N., Regev, A., 2011. Full-length transcriptome assembly from RNA-Seq data without a – 1257785 and DEB-1258205). Collecting was conducted under permits reference genome. Nat. Biotechnol. 29, 644 652. http://dx.doi.org/10.1038/nbt. 1883. granted by SEMARNAT to RWB, the late F. Mendoza-Quijano, D. Hime, P.M., Hotaling, S., Grewelle, R.E., O’Neill, E.M., Voss, S.R., Shaffer, H.B., Weisrock, Lazcano, and UNAM. For additional support, we thank members of the D.W., 2016. The influence of locus number and information content on species de- McCormack and Klicka Labs, C. Franklin, and D. Lazcano. limitation: an empirical test case in an endangered Mexican . Mol. Ecol. 25, 5959–5974. http://dx.doi.org/10.1111/mec.13883. Hosner, P.A., Faircloth, B.C., Glenn, T.C., Braun, E.L., Kimball, R.T., 2016. Avoiding Appendix A. Supplementary material missing data biases in phylogenomic inference: an empirical study in the landfowl (Aves: Galliformes). Mol. Biol. Evol. 33, 1110–1125. http://dx.doi.org/10.1093/ molbev/msv347. Supplementary data associated with this article can be found, in the Katoh, K., Standley, D.M., 2013. MAFFT multiple sequence alignment Software Version 7: online version, at https://doi.org/10.1016/j.ympev.2018.03.024. improvements in performance and usability. Mol. Biol. Evol. 30, 772–780. http://dx. doi.org/10.1093/molbev/mst010. Lemey, P., Rambaut, A., Drummond, A.J., Suchard, M.A., 2009. Bayesian phylogeography References finds its roots. PLOS Comput. Biol. 5, e1000520. http://dx.doi.org/10.1371/journal. pcbi.1000520. Badillo-Saldaña, L.M., Ramírez-Bautista, A., Berriozabal-Islas, C., Beteta-Hernández, C.I., Lemey, P., Rambaut, A., Welch, J.J., Suchard, M.A., 2010. Phylogeography takes a re- – 2015. Range extension of the Giant Salamander, Pseudoeurycea gigantea (Taylor 1938) laxed random walk in continuous space and time. Mol. Biol. Evol. 27, 1877 1885. (Caudata: Pletodontidae), and some aspects of its natural history within Hidalgo http://dx.doi.org/10.1093/molbev/msq067. state, Mexico. Check List 11, 1521. http://dx.doi.org/10.15560/11.1.1521. Lips, K.R., Burrowes, P.A., Mendelson, J.R., Parra-Olea, G., 2005. Amphibian declines in Ballard, J.W.O., Whitlock, M.C., 2004. The incomplete natural history of mitochondria. Latin America: widespread population declines, extinctions, and impacts. Biotropica – Mol. Ecol. 13, 729–744. http://dx.doi.org/10.1046/j.1365-294X.2003.02063.x. 37, 163 165. http://dx.doi.org/10.2307/30043168. ff Bielejec, F., Rambaut, A., Suchard, M.A., Lemey, P., 2011. SPREAD: spatial phylogenetic McCartney-Melstad, E., Mount, G.G., Sha er, H.B., 2016. Exon capture optimization in – reconstruction of evolutionary dynamics. Bioinformatics 27, 2910–2912. http://dx. amphibians with large genomes. Mol. Ecol. Resour. 16, 1084 1094. http://dx.doi. doi.org/10.1093/bioinformatics/btr481. org/10.1111/1755-0998.12538. Bolger, A.M., Lohse, M., Usadel, B., 2014. Trimmomatic: a flexible trimmer for Illumina McCormack, J.E., Tsai, W.L.E., Faircloth, B.C., 2016. Sequence capture of ultraconserved – sequence data. Bioinformatics 30, 2114–2120. http://dx.doi.org/10.1093/ elements from bird museum specimens. Mol. Ecol. Resour. 16, 1189 1203. http://dx. bioinformatics/btu170. doi.org/10.1111/1755-0998.12466. ’ Brown, W., George, M., Wilson, A.C., 1979. Rapid evolution of mitochondrial Metcalfe, S.E., O Hara, S.L., Caballero, M., Davies, S.J., 2000. Records of Late Pleistocene- — – DNA. Proc. Natl. Acad. Sci. USA 76, 1967–1971. Holocene climatic change in Mexico a review. Quat. Sci. Rev. 19, 699 721. http:// Bryson, R.W., Smith, B.T., Nieto-Montes de Oca, A., García-Vázquez, U.O., Riddle, B.R., dx.doi.org/10.1016/S0277-3791(99)00022-0. 2014. The role of mitochondrial introgression in illuminating the evolutionary his- Mulcahy, D.G., Morrill, B.H., Mendelson, J.R., 2006. Historical biogeography of lowland tory of Nearctic treefrogs. Zool. J. Linn. Soc. 172, 103–116. http://dx.doi.org/10. species of toads (Bufo) across the Trans-Mexican Neovolcanic Belt and the Isthmus of – 1111/zoj.12169. Tehuantepec. J. Biogeogr. 33, 1889 1904. Burleigh, J.G., Kimball, R.T., Braun, E.L., 2015. Building the avian tree of life using a Newman, C.E., Austin, C.C., 2016. Sequence capture and next-generation sequencing of – large-scale, sparse supermatrix. Mol. Phylogenet. Evol. 84, 53–63. http://dx.doi.org/ ultraconserved elements in a large-genome salamander. Mol. Ecol. 25, 6162 6174. 10.1016/j.ympev.2014.12.003. http://dx.doi.org/10.1111/mec.13909. Corona, A.M., Toledo, V.H., Morrone, J.J., 2007. Does the Trans-mexican Volcanic Belt Olmo, E., 1991. Genome variations in the transition from amphibians to reptiles. J. Mol. – represent a natural biogeographical unit? An analysis of the distributional patterns of Evol. 33, 68 75. http://dx.doi.org/10.1007/BF02100197. Coleoptera. J. Biogeogr. 34, 1008–1015. http://dx.doi.org/10.1111/j.1365-2699. Palacios-Aguilar, R., Santos-Bibiano, R., Beltrán-Sánchez, E., 2016. Notable distributional 2006.01666.x. records of amphibians and reptiles from Guerrero Mexico. Mesoam. Herpetol. 3, – Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., 2012. Bayesian phylogenetics with 527 531. fi BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973. http://dx.doi.org/10. Parra-Olea, G., Flores-Villela, O., Mendoza-Almeralla, C., 2014. Biodiversidad de an bios – 1093/molbev/mss075. en México. Rev. mex. biodivers. 85, S460 S466. http://dx.doi.org/10.7550/rmb. Faircloth, B.C., 2016. PHYLUCE is a software package for the analysis of conserved 32027. genomic loci. Bioinformatics 32, 786–788. http://dx.doi.org/10.1093/ Parra-Olea, G., Garcia-Paris, M., Papenfuss, T.J., Wake, D.B., 2005. Systematics of the bioinformatics/btv646. Pseudoeurycea bellii (Caudata: ) species complex. Herpetologica 61, – Faircloth, B.C., 2013a. Illumina TruSeq Library Prep for Target Enrichment. Available 145 158. http://dx.doi.org/10.1655/03-02. ff from < http://www.ultraconserved.org >. Parra-Olea, G., Wake, D., Ra aelli, J., Papenfuss, T., 2008. Pseudoeurycea naucampatepetl. Faircloth, B.C., 2013b. Illumiprocessor: A Trimmomatic Wrapper for Parallel Adapter and The IUCN Red List of Threatened Species 2008: e.T59389A11914996. doi:10.2305/ Quality Trimming. < https://github.com/faircloth-lab/illumiprocessor/ >. IUCN.UK.2008.RLTS.T59389A11914996.en. fi Faircloth, B.C., 2012. Target enrichment of Illumina libraries. Available from < http:// Parra-Olea, G., Wind eld, J.C., Velo-Antón, G., Zamudio, K.R., 2012. Isolation in habitat fi www.ultraconserved.org >. refugia promotes rapid diversi cation in a montane tropical salamander. J. Biogeogr. – Faircloth, B.C., McCormack, J.E., Crawford, N.G., Harvey, M.G., Brumfield, R.T., Glenn, 39, 353 370. http://dx.doi.org/10.1111/j.1365-2699.2011.02593.x. T.C., 2012. Ultraconserved elements anchor thousands of genetic markers spanning Rambaut, A., Drummond, A.J., 2007. Tracer 1.6. < http://beast.bio.ed.ac.uk/Tracer >.

83 R.W. Bryson et al. Molecular Phylogenetics and Evolution 125 (2018) 78–84

Rovito, S.M., Parra-Olea, G., Hanken, J., Bonett, R.M., Wake, D.B., 2013. Adaptive ra- Biodivers. 12, 1–22. http://dx.doi.org/10.1080/14772000.2014.882428. diation in miniature: the minute salamanders of the Mexican highlands (Amphibia: Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular Plethodontidae: Thorius). Biol. J. Linn. Soc. Lond. 109, 622–643. http://dx.doi.org/ evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729. http://dx. 10.1111/bij.12083. doi.org/10.1093/molbev/mst197. Rovito, S.M., Parra-Olea, G., Recuero, E., Wake, D.B., 2015. Diversification and biogeo- Toews, D.P.L., Brelsford, A., 2012. The biogeography of mitochondrial and nuclear dis- graphical history of Neotropical plethodontid salamanders. Zool. J. Linn. Soc. 175, cordance in . Mol. Ecol. 21, 3907–3930. http://dx.doi.org/10.1111/j.1365- 167–188. http://dx.doi.org/10.1111/zoj.12271. 294X.2012.05664.x. Rovito, S.M., Parra-Olea, G., Vásquez-Almazán, C.R., Luna-Reyes, R., Wake, D.B., 2012. Velo-Antón, G., Parra, J.L., Parra-Olea, G., Zamudio, K.R., 2013. Tracking climate change Deep divergences and extensive phylogeographic structure in a clade of lowland in a dispersal-limited species: reduced spatial and genetic connectivity in a montane tropical salamanders. BMC Evol. Biol. 12, 255. http://dx.doi.org/10.1186/1471- salamander. Mol. Ecol. 22, 3261–3278. http://dx.doi.org/10.1111/mec.12310. 2148-12-255. Wilson, L.D., Johnson, J.D., Mata-Silva, V., 2013. A conservation reassessment of the Sandoval-Comte, A., Pineda, E., Rovito, S.M., Luría-Manzano, R., 2017. A new species of amphibians of Mexico based on the EVS measure. Amphib. Reptile Conserv. 7, 9–127. Isthmura (Caudata: Plethodontidae) from the montane cloud forest of central Zarza, E., Connors, E.M., Maley, J.M., Tsai, W.L.E., Heimes, P., Kaplan, M., McCormack, J. Veracruz, Mexico. Zootaxa 4277, 573–582. http://dx.doi.org/10.11646/zootaxa. E., 2017. Bridging multilocus species delimitation and DNA barcoding through target 4277.4.7. enrichment of UCEs: A case study with Mexican highland frogs. bioRxiv 153601. Smith, B.T., Harvey, M.G., Faircloth, B.C., Glenn, T.C., Brumfield, R.T., 2014. Target doi:10.1101/153601. capture and massively parallel sequencing of ultraconserved elements for compara- Zarza, E., Faircloth, B.C., Tsai, W.L.E., Bryson, R.W., Klicka, J., McCormack, J.E., 2016. tive studies at shallow evolutionary time scales. Syst. Biol. 63, 83–95. http://dx.doi. Hidden histories of gene flow in highland birds revealed with genomic markers. Mol. org/10.1093/sysbio/syt061. Ecol. 25, 5144–5157. http://dx.doi.org/10.1111/mec.13813. Streicher, J.W., García-Vázquez, U.O., Ponce-Campos, P., Flores-Villela, O., Campbell, Zink, R.M., Barrowclough, G.F., 2008. Mitochondrial DNA under siege in avian phylo- J.A., Smith, E.N., 2014. Evolutionary relationships amongst polymorphic direct-de- geography. Mol. Ecol. 17, 2107–2121. veloping frogs in the Craugastor rhodopis Species Group (Anura: Craugastoridae). Syst.

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