Brett R. Riddle

MITOCHONDRIAL INTROGRESSION AND INCOMPLETE LINEAGE SORTING THROUGH SPACE AND TIME: PHYLOGENETICS OF CROTAPHYTID LIZARDS

Abstract We investigate the roles of mitochondrial introgression and incomplete lineage sorting during the phylogenetic history of crotaphytid lizards. Our Bayesian phylogenetic estimate for Crotaphytidae is based on analysis of mitochondrial DNA sequence data for 408 individuals representing the 12 extant species of Crotaphytus and Gambelia. The mitochondrial phylogeny disagrees in several respects with a previously published morphological tree, as well as with conventional species designations, and we conclude that some of this disagreement stems from hybridization-mediated mitochondrial introgression, as well as from incomplete lineage sorting. Unidirectional introgression of Crotaphytus collaris (western collared lizard) mitochondria into C. reticulatus (reticulate collared lizard) populations in the Rio Grande Valley of Texas has resulted in the replacement of ancestral C. reticulatus mitochondria over approximately two-thirds of the total range of the species, a linear distance of ∼270 km. Introgression of C. collaris mitochondria into C. bicinctores (Great Basin collared lizard) populations in southwestern Arizona requires a more complex scenario because at least three temporally separated and superimposed introgression events appear to have occurred in this region. We propose an “introgression conveyor” model to explain this unique pattern of mitochondrial variation in this region. We show with ecological niche modeling that the predicted geographical ranges of C. collaris, C. bicinctores, and C. reticulatus during glacial maxima could have provided enhanced opportunities for past hybridization. Our analyses suggest that incomplete lineage sorting and/or introgression has further confounded the phylogenetic placements of additional species including C. nebrius, C. vestigium, C. insularis, C. grismeri, and perhaps G. copei. Despite many independent instances of interspecific hybridization among crotaphytid lizards, the species continue to maintain morphological and geographic cohesiveness throughout their ranges.

The molecular phylogeographic bridge between deep and shallow history in continental biotas

Recent studies have provided evidence that species diversity and distributions in continental biotas reflect a long history of responses (e.g. range shifts, speciation or adaptation) to habitat changes produced by geological activity over the past several million years (deep time) as well as glacial-interglacial cycles over the most recent hundreds of thousands of years (shallow time). Molecular sequences in extant taxa can be used to infer speciation and biogeographic history in deep time, as well as changes in population distributions produced by range shifts in shallow time, and thus provide a basis for constructing bridges between historical biogeographic, paleoecological and ecological biogeographic perspectives. References.

Molecular Biogeography in the Pocket Mice (Perognathus and Chaetodipus) and Grasshopper Mice (Onychomys): the Late Cenozoic Development of a North American Aridlands Rodent Guild

Paleoecological and geological evidence previously have been used to infer a sequential development of arid landscapes in western North America composed of: a gradual Miocene development of savanna and semidesert habitats; a rapid late-Miocene expansion of regional deserts, grasslands, and shrubsteppes; cyclical late Pliocene-Pleistocene changes in the distribution and composition of aridlands biotas. Rodents that characterize aridlands regions in western North America include lineages detectable in the fossil record back to the late Oligocene as well as mid-Miocene immigrants from Asia. In this study, nucleotide-sequence data from the mitochondrial DNA genes COIII and cytochrome b were used to analyze phylogeny, genetic divergence, and geographic structure within the pocket mice ( Perognathus and Chaetodipus ) and grasshopper mice ( Onychomys ). Molecular phylogenies, estimates of divergence times, and geographic distributions suggest that middle to late Pleistocene glacial cycles appear to have had little influence on lineage divergence in aridlands rodents. Rather, a correspondence between molecular, distributional, paleoecological, and geological evidence suggests that divergence and current distributions of most extant lineages can be attributed to late Tertiary-early Quaternary development of the western North American cordillera. These data are used to produce a predictive generalized model of late Cenozoic area relationships among arid regions in western North America.

Cryptic Neogene vicariance and Quaternary dispersal of the red-spotted toad ( Bufo punctatus ): insights on the evolution of North American warm desert biotas

We define the geographical distributions of mitochondrial DNA (mtDNA) lineages embedded within a broadly distributed, arid‐dwelling toad, Bufo punctatus. These patterns were evaluated as they relate to hypothesized vicariant events leading to the formation of desert biotas within western North America. We assessed mtDNA sequence variation among 191 samples from 82 sites located throughout much of the species’ range. Parsimony‐based haplotype networks of major identified lineages were used in nested clade analysis (NCA) to further elucidate and evaluate shallow phylogeographic patterns potentially associated with Quaternary (Pleistocene–Holocene) vicariance and dispersal. Phylogenetic analyses provided strong support for three monophyletic lineages (clades) within B. punctatus. The geographical distributions of the clades showed little overlap and corresponded to the general boundaries of the Peninsular Desert, and two continental desert regions, Eastern (Chihuahuan Desert–Colorado Plateau) and Western (Mojave–Sonoran deserts), geographically separated along the Rocky Mountains and Sierra Madre Occidental. The observed divergence levels and congruence with postulated events in earth history implicate a late Neogene (latest Miocene–early Pliocene) time frame for separation of the major mtDNA lineages. Evaluation of nucleotide and haplotype diversity and interpretations from NCA reveal that populations on the Colorado Plateau resulted from a recent, likely post‐Pleistocene, range expansion from the Chihuahuan Desert. Dispersal across historical barriers separating major continental clades appear to be recent, resulting in secondary contacts in at least two areas. Given the observed contact between major clades, we speculated as to why the observed deep phylogeographic structure has not been eroded during the multiple previous interglacials of the Pleistocene.

HISTORICAL BIOGEOGRAPHY IN NORTH AMERICAN ARID REGIONS: AN APPROACH USING MITOCHONDRIAL-DNA PHYLOGENY IN GRASSHOPPER MICE (GENUS ONYCHOMYS )

Restriction‐endonuclease‐site variation of mitochondrial DNA (mtDNA) was used to investigate patterns of geographic and phylogenetic divergence within the rodent genus Onychomys. Onychomys has occupied arid habitats in the western North American deserts, shrub‐steppes, and grasslands since the late Tertiary. A phylogenetic analysis of the total mtDNA restriction‐site variation throughout the range of Onychomys suggests that the distribution of this genus has been affected by the same Quaternary pluvial‐interpluvial climatic fluctuations that have resulted in the periodic fragmentation of arid habitats in western North America. Onychomys mtDNA haplotypes define at least five discrete geographical subsets, suggesting that there are five areas of endemism for biota restricted to arid and semiarid habitats in North America. The mtDNA‐haplotype phylogeny can be used to infer an hypothesis of historical relationships among the five areas of endemism as follows: ([{(Wyoming Basin + Interior Plains + Colorado Plateaus) + (Columbia Basin + Great Basin)} + Gulf Coastal Plain] + Chihuahuan) + Western Deserts. The results of this study point to the potential use of mtDNA‐haplotype phylogenies to reconstruct historical biogeographic events in Quaternary time. The utility of mtDNA variation depends in part on the ecology and distribution of the species being examined. Therefore, our hypothesized area cladogram can be tested by investigating regional relationships in other western North American taxa with distributions similar to Onychomys.

Phylogeography of the mountain chickadee (Poecile gambeli): diversification, introgression, and expansion in response to Quaternary climate change

Since the late 1990s, molecular techniques have fuelled debate about the role of Pleistocene glacial cycles in structuring contemporary avian diversity in North America. The debate is still heated; however, there is widespread agreement that the Pleistocene glacial cycles forced the repeated contraction, fragmentation, and expansion of the North American biota. These demographic processes should leave genetic ‘footprints’ in modern descendants, suggesting that detailed population genetic studies of contemporary species provide the key to elucidating the impact of the late Quaternary (late Pleistocene–Holocene). We present an analysis of mitochondrial DNA (mtDNA) variation in the mountain chickadee (Poecile gambeli) in an attempt to examine the genetic evidence of the impact of the late Quaternary glacial cycles. Phylogenetic analyses reveal two strongly supported clades of P. gambeli: an Eastern Clade (Rocky Mountains and Great Basin) and a Western Clade (Sierra Nevada and Cascades). Post‐glacial introgression is apparent between these two clades in the Mono Lake region of Central California. Within the Eastern Clade there is evidence of isolation‐by‐distance in the Rocky Mountain populations, and of limited gene flow into and around the Great Basin. Coalescent analysis of genetic variation in the Western Clade indicates that northern (Sierra Nevada/Cascades) and southern (Transverse/Peninsular Ranges) populations have been isolated and evolving independently for nearly 60 000 years.

BASAL CLADES AND MOLECULAR SYSTEMATICS OF HETEROMYID RODENTS

Abstract The New World rodent family Heteromyidae shows a marvelous array of ecomorphological types, from bipedal, arid-adapted forms to scansorial, tropical-adapted forms. Although recent studies have resolved most of the phylogenetic relationships among heteromyids at the shallower taxonomic levels, fundamental questions at the deeper taxonomic levels remain unresolved. This study relies on DNA sequence information from 3 relatively slowly evolving mitochondrial genes, cytochrome c oxidase subunit I, 12S, and 16S, to examine basal patterns of phylogenesis in the Heteromyidae. Because slowly evolving mitochondrial genes evolve and coalesce more rapidly than most nuclear genes, they may be superior to nuclear genes for resolving short, basal branches. Our molecular data (2,381 base pairs for the 3-gene data set) affirm the monophyly of the family and resolve the major basal clades in the family. Alternative phylogenetic hypotheses of subfamilial relationships are examined statistically and the Perognathinae and Heteromyinae are found to represent sister clades relative to the Dipodomyinae. The 3 traditional subfamilial groupings are supported; the controversial placement of Microdipodops as a sister clade to Dipodomys in the Dipodomyinae is affirmed, Perognathus and Chaetodipus are distinct sister clades within the Perognathinae, and species of Liomys and Heteromys form the resolved clade Heteromyinae. However, Liomys is found to be paraphyletic relative to Heteromys and, given that this finding corroborates earlier studies, we present a formal taxonomy of Heteromys wherein we place Liomys in synonymy. Semiparametric and parametric methods are used to estimate divergence times from our molecular data and a chronogram of the Heteromyidae, calibrated by the oldest known fossils of Dipodomys and Perognathus, is presented. Our time estimates reveal subfamilial differentiation in the early Miocene (22.3–21.8 million years ago) and pose testable times of divergence for the basal heteromyid nodes. With the basal heteromyid clades resolved and cladogenic events positioned in a time framework, we review the major geological and paleoecological events of the Oligocene and Miocene associated with the early historical biogeography of the family.

Pleistocene Impacts on the Phylogeography of the Desert Pocket Mouse (Chaetodipus penicillatus)

Abstract The desert pocket mouse (Chaetodipus penicillatus) comprises 6 nominate subspecies that occupy warm, sandy desert-scrub habitats across the Mojave and Sonoran deserts. The most thorough morphological assessment within the species noted variable levels of distinctiveness, leading to uncertainty regarding the geographic distributions of subspecies. Subsequent genetic assessments using chromosomal, allozymic, and mitochondrial DNA (mtDNA) sequence data detected a general east–west divergence centered on the Colorado River, but few locations were included in these assessments. We investigated phylogeographic structure in C. penicillatus by sequencing regions of mtDNA for 220 individuals from 51 locations representing all continental subspecies. We identify 2 major monophyletic mtDNA lineages (clades) roughly centered in the Mojave and Sonoran deserts. These clades broadly overlap along the Lower Colorado River valley and adjacent desert regions across most of the range of C. p. penicillatus. Outside this zone of mtDNA clade overlap, Sonoran clade haplotypes occur in populations from across the range of C. p. pricei and extend to the northwestern edge of the Sonoran Desert within the southern range of C. p. angustirostris. Northern clade haplotypes occur in populations within the ranges of C. p. sobrinus and C. p. stephensi and in populations from the western Mojave Desert in the northern range of C. p. angustirostris. Based on rough estimates for rates of sequence evolution, divergence among the major clades appears to have occurred during the Pleistocene, but well before the latest glacial maximum. The secondary contact among the major clades appears to have some longevity, with little evidence of recent, postglacial range expansion. We develop ecological niche models (EMNs) for the major lineages of C. penicillatus, and project these models onto reconstructions of climatic conditions during the latest glacial maximum (LGM; 18,000–21,000 years ago). The ENMs for each clade indicate differences in predicted current geographic distributions as well as distributions during the LGM. Models for the LGM indicate broad retention of potential habitat within the area of contact among the major clades. Furthermore, the ENM for the Mojave clade in particular indicates retention of suitable habitat during the LGM in small isolated patches within northern areas, consistent with the haplotype network that supports the perspective that some populations from the Mojave clade were isolated within northern refugia during the last glacial period.

Phylogenetics of the new world rodent family heteromyidae

Abstract The family Heteromyidae includes 6 genera of rodents traditionally placed in 3 subfamilies endemic to the Nearctic and northern Neotropical biogeographic regions. Although several of these taxa represent intensively studied members of North and Central American ecosystems (e.g., kangaroo rats and pocket mice), phylogenetic relationships within and among subfamilies, genera, and species-groups are not well understood. Here, we used maximum-likelihood, Bayesian, and maximum parsimony analyses of sequence data from 2 mitochondrial DNA genes, the cytochrome oxidase subunit 3 gene (699 base pairs [bp]) and the cytochrome-b gene (1,140 bp), to investigate phylogenetic relationships among 55 species-level taxa. We found robust support for monophyly of genera Dipodomys, Microdipodops, Chaetodipus, and Perognathus; sampling of Liomys and Heteromys was inadequate to evaluate their reciprocal status. All analyses converge on a phylogeny that robustly resolves several historically contentious issues, including monophyly of the subfamily Dipodomyinae (Microdipodops plus Dipodomys), and a monophyletic Chaetodipus that includes C. formosus, C. baileyi, C. rudinoris, and C. hispidus. However, Perognathinae (Perognathus plus Chaetodipus) is not supported, with no basal resolution among Perognathus, Chaetodipus, Dipodomyinae, and Heteromyinae. Many intrageneric clades receive strong support and are discussed herein. Although phylogenetic resolution is limited at the basal nodes of the Heteromyidae radiation, our results provide a basis for developing a provisional hypothesis regarding the historical biogeography in combination with independent information on the Neogene geological history of western North America and the fossil record of the family.

ELUCIDATION OF CRYPTIC DIVERSITY IN A WIDESPREAD NEARCTIC TREEFROG REVEALS EPISODES OF MITOCHONDRIAL GENE CAPTURE AS FROGS DIVERSIFIED ACROSS A DYNAMIC LANDSCAPE

We investigate the evolutionary history of the wide‐ranging Nearctic treefrog Hyla arenicolor through the integration of extensive range‐wide sampling, phylogenetic analyses of multilocus genetic data, and divergence dating. Previous phylogeographic studies of this frog documented a potential signature of introgressive hybridization from an ecologically and morphologically divergent sister species. Based on our Bayesian phylogenetic analyses of mitochondrial DNA, we inferred strong phylogeographic structure in H. arenicolor as indicated by seven well‐supported clades, five of which correspond to well‐defined biogeographic regions. Clades from the Balsas Basin and southwestern Central Mexican Plateau in Mexico, and the Grand Canyon of Arizona, group with the morphologically, behaviorally, and ecologically divergent mountain treefrogs in the H. eximia group, rendering H. arenicolor as paraphyletic. The phylogenetic position of at least two of these three H. arenicolor clades within the H. eximia group, however, is most likely the result of several episodes of introgressive hybridization and subsequent mitochondrial gene capture separated in time and space, as supported by evidence from the nuclear genes. Hyla arenicolor from the Balsas Basin appear to be deeply divergent from other H. arenicolor and represent a distinctly different species. Results suggests that introgressive hybridization events, both ancient and contemporary, coupled with late Neogene vicariance and Pleistocene climate‐driven range shifts, have all played a role in the historical diversification of H. arenicolor.