A phylogenomic perspective on the biogeography of skinks in the Plestiodon brevirostris group inferred from target enrichment of ultraconserved elements

Abstract

Aim The aim of our study was to reconstruct ancestral geographic distributions from time‐calibrated phylogenies generated from phylogenomic data to answer three broad questions about the biogeography of skinks in the Plestiodon brevirostris group: (1) Are biogeographic patterns correlated with the formation of the Trans‐Mexican Volcanic Belt? (2) Do different methods of phylogenetic estimation result in different topologies? If so, (3) are biogeographic reconstructions impacted by the use of different phylogenetic trees? Location Mexico. Methods We used target enrichment of ultraconserved elements (UCEs) to obtain sequence data from 58 skinks representing 11 of the 13 described species in the group. We estimated time‐calibrated phylogenies using concatenated and multispecies coalescent phylogenetic approaches. We used these phylogenies to reconstruct ancestral geographic distributions. Results The final dataset contained 3,282 UCEs from each skink. Samples of each putative species formed well‐supported clades in phylogenetic trees. Time‐calibrated phylogenies estimated using concatenated and multispecies coalescent methods were generally congruent, but differed in the placement of one basal relationship. Divergences in the P. brevirostris group were temporally and spatially congruent with the pre‐Pleistocene formation of the Trans‐Mexican Volcanic Belt. The group most likely colonized the Mexican highlands from east to west during the Late Miocene and Pliocene. Inferences about the early biogeographic history of the group were confounded by the unresolved placement of a key phylogenetic relationship deep in the phylogeny. Conclusions Skinks in the P. brevirostris group represent another example of a widespread montane Mexican taxon with a long history of pre‐Pleistocene diversification associated with the primary formation of the Trans‐Mexican Volcanic Belt. This mountain range seems to have been both a cradle of diversification for P. brevirostris group species and a land bridge facilitating dispersal across the Mexican highlands. Our results highlight the probable existence of new species within the P. brevirostris complex and suggest that querying a large portion of the genome may be critically important for studying the biogeographic history of these skinks. However, inferred differences between the concatenated and multispecies coalescent phylogenies, and the different biogeographic histories of the P. brevirostris group reconstructed from these phylogenies, caution that methods of estimating phylogenetic trees used in biogeographic reconstructions need to be carefully considered.

High genetic diversity and stable Pleistocene distributional ranges in the widespread Mexican red oak Quercus castanea Née (1801) (Fagaceae)

“…Finally, our results indicate a similar pattern to previous studies in the Mexican highlands that have reported pre‐Quaternary divergence times (Bryson et al, 2017, 2018; Bryson & Riddle, 2012; Ornelas & González, 2014) and to patterns of pre‐Quaternary diversification for Neotropical species, characterized by complex mixtures of taxa that radiated and spread over a wide range of timescales (Bennett et al, 2012). These findings indicate that the origin and maintenance of a large proportion of the genetic diversity in Q. castanea have occurred within the Trans‐Mexican Volcanic Belt, which is also a hotspot for oak species diversity and has acted as a natural bridge between other biogeographic provinces (Bryson et al, 2018).…”

“…The analysis of the evolutionary patterns reported for the Mexican Highlands (e.g., Bryson, Linkem, & Pavón‐Vázquez, 2017; Bryson et al, 2018; Caviedes‐Solis & Leaché, 2018; Sanginés‐Franco et al, 2015; Villaseñor, Delgadillo, & Ortiz, 2006) have allowed to state hypothesis that describe the evolution of montane forests (e.g., cloud forest by Ramírez‐Barahona & Eguiarte, 2013), to describe common phylogeographical breaks limiting the species genetic structure and gene flow during different periods (Ornelas et al, 2013), and to propose the expected patterns of genetic variation in a heterogeneous geological framework mostly drove by volcanism (Mastretta‐Yanes et al, 2015). Such studies clearly illustrate the still incipient understanding of the biota evolution in a transition zone between the Nearctic and Neotropics.…”

Cryptic diversity in the Mexican highlands: Thousands of UCE loci help illuminate phylogenetic relationships, species limits and divergence times of montane rattlesnakes (Viperidae: Crotalus)

“…Genomic DNA was extracted from tissue samples using the Qiagen DNeasy Blood & Tissue Kit (Qiagen Inc., Valencia, CA, USA). Aliquots of extracts were shipped to RAPiD Genomics (Gainsville, FL, USA) for UCE library preparation and sequencing following Bryson et al (). Briefly, 5,472 custom‐designed probes (MYbaits; MYcroarray, Inc., Ann Arbor, MI, USA) were used to enrich 5,060 UCE loci using protocols specified in Faircloth et al ().…”

“…Libraries were sequenced on an Illumina HiSeq 3,000 (100 paired‐end) at the University of Florida ICBR Facility. Data quality filtering and assembly were performed using the phyluce pipeline (Faircloth, ) following Bryson et al (). A locus was retained in the final assembly if it was represented by >75% of taxa.…”

Combining ultraconserved elements and mtDNA data to uncover lineage diversity in a Mexican highland frog (Sarcohyla; Hylidae)

“…It occurs in several mountain ranges in central Mexico separated by lowland barriers and might therefore consist of multiple distinct lineages or even species. Studies of many broadly distributed highland species across this region have revealed cryptic lineages (McCormack et al, 2008; Bryson et al, 2011; Leaché et al, 2013; Navarro-Sigüenza, García-Hernández & Peterson, 2013; Mastretta-Yanes et al, 2015; Bryson Jr et al, 2017), some later described at the species level. Amphibians, it seems, are especially prone to under-splitting in the Mexican Highlands (Rovito et al, 2012; Rovito et al, 2013; Bryson Jr et al, 2018).…”