Chris J. Conroy

Genetic Response to Climatic Change: Insights from Ancient DNA and Phylochronology

Understanding how climatic change impacts biological diversity is critical to conservation. Yet despite demonstrated effects of climatic perturbation on geographic ranges and population persistence, surprisingly little is known of the genetic response of species. Even less is known over ecologically long time scales pertinent to understanding the interplay between microevolution and environmental change. Here, we present a study of population variation by directly tracking genetic change and population size in two geographically widespread mammal species (Microtus montanus and Thomomys talpoides) during late-Holocene climatic change. We use ancient DNA to compare two independent estimates of population size (ecological and genetic) and corroborate our results with gene diversity and serial coalescent simulations. Our data and analyses indicate that, with population size decreasing at times of climatic change, some species will exhibit declining gene diversity as expected from simple population genetic models, whereas others will not. While our results could be consistent with selection, independent lines of evidence implicate differences in gene flow, which depends on the life history strategy of species.

Multiple geographic origins of commensalism and complex dispersal history of black rats

The Black Rat (Rattus rattus) spread out of Asia to become one of the worlds worst agricultural and urban pests, and a reservoir or vector of numerous zoonotic diseases, including the devastating plague. Despite the global scale and inestimable cost of their impacts on both human livelihoods and natural ecosystems, little is known of the global genetic diversity of Black Rats, the timing and directions of their historical dispersals, and the risks associated with contemporary movements. We surveyed mitochondrial DNA of Black Rats collected across their global range as a first step towards obtaining an historical genetic perspective on this socioeconomically important group of rodents. We found a strong phylogeographic pattern with well-differentiated lineages of Black Rats native to South Asia, the Himalayan region, southern Indochina, and northern Indochina to East Asia, and a diversification that probably commenced in the early Middle Pleistocene. We also identified two other currently recognised species of Rattus as potential derivatives of a paraphyletic R. rattus. Three of the four phylogenetic lineage units within R. rattus show clear genetic signatures of major population expansion in prehistoric times, and the distribution of particular haplogroups mirrors archaeologically and historically documented patterns of human dispersal and trade. Commensalism clearly arose multiple times in R. rattus and in widely separated geographic regions, and this may account for apparent regionalism in their associated pathogens. Our findings represent an important step towards deeper understanding the complex and influential relationship that has developed between Black Rats and humans, and invite a thorough re-examination of host-pathogen associations among Black Rats.

Extracting time from phylogenies: Positive interplay between fossil and genetic data

Abstract Temporal information on mammalian evolution allows testing of hypotheses about the mode of speciation and extinction, comparison of rates of evolution across taxa, and correlation of cladogenesis with important geological processes. Important insights can be made from combining data from fossils and molecules (DNA sequences), and relevant methods are expanding. When considering these methods, careful consideration should be given to features affecting time estimation (e.g., accuracy of tree construction, branch length estimation, taxonomic and genomic sampling, and sources of genetic and calibration errors). We report on the available methods that aid in evolutionary time estimation from molecular data and corresponding fossils. We recommend several steps to improve this process. First, we recommend using appropriate DNA substitution models to help correct DNA distance estimates and construct trees with more reliable branch lengths. Second, we recommend using multiple fossil calibration dates where possible. Third, in general, we recommend a conservative approach to time estimation by reporting inherent errors associated with genetic distances, calibration selection and application. In conclusion, temporal data derived from molecular clocks should be regarded in light of their dependence on paleontological information and their synergy with fossil data rather than competing with paleontological information. Thus, despite the varied sources of error, we encourage the extraction of time from molecular data with careful examination of potential biases.

Invasion facilitates hybridization with introgression in the Rattus rattus species complex

Biological invasions result in novel species interactions, which can have significant evolutionary impacts on both native and invading taxa. One evolutionary concern with invasions is hybridization among lineages that were previously isolated, but make secondary contact in their invaded range(s). Black rats, consisting of several morphologically very similar but genetically distinct taxa that collectively have invaded six continents, are arguably the most successful mammalian invaders on the planet. We used mitochondrial cytochrome b sequences, two nuclear gene sequences (Atp5a1 and DHFR) and nine microsatellite loci to examine the distribution of three invasive black rat lineages (Rattus tanezumi, Rattus rattus I and R. rattus IV) in the United States and Asia and to determine the extent of hybridization among these taxa. Our analyses revealed two mitochondrial lineages that have spread to multiple continents, including a previously undiscovered population of R. tanezumi in the south‐eastern United States, whereas the third lineage (R. rattus IV) appears to be confined to Southeast Asia. Analyses of nuclear DNA (both sequences and microsatellites) suggested significant hybridization is occurring among R. tanezumi and R. rattus I in the United States and also suggest hybridization between R. tanezumi and R. rattus IV in Asia, although further sampling of the latter species pair in Asia is required. Furthermore, microsatellite analyses suggest unidirectional introgression from both R. rattus I and R. rattus IV into R. tanezumi. Within the United States, introgression appears to be occurring to such a pronounced extent that we were unable to detect any nuclear genetic signal for R. tanezumi, and a similar pattern was detected in Asia.

Phylogeographic Study of the California Vole, Microtus californicus

Abstract Many vertebrate taxa show genetic differentiation between populations in northern and southern California. This genetic pattern may reflect a common environmental history for these species. For example, a previous study of the California vole (Microtus californicus) showed morphological divergence between populations in northern and southern California and decreased fertility in crosses between the populations. To investigate phylogeographic differences in this species, we assessed variation in mitochondrial and nuclear DNA throughout much of its distribution from Oregon to Baja California. We generated molecular data (mitochondrial cytochrome b and nuclear acid phosphatase V intron [AP5]) for 178 individuals. Examination of these data suggests 2 phylogeographic groups that are largely discordant with the boundaries of 17 currently recognized subspecies. Estimates of pairwise genetic divergence between these groups for cytochrome b are as high as 4.46% uncorrected p. Sequence data for AP5 also indicate a division between populations of M. californicus in northern and southern California. Examination of data from the mitochondrial and nuclear markers together suggests limited gene flow between clades. These data are concordant with other studies that suggest that mountain ranges in California were important in within- and possibly between-species divergence and subsequent contact. The general distribution of each clade, combined with a geographic information system analysis of known capture sites, suggests that clade divergence may be correlated with ecological differences. Our study creates a new framework for reevaluating morphological and ecological diversity in this species, and with more diverse markers, possibly the recognition of 2 species of California voles.

Cryptic genetic diversity in Rattus of the San Francisco Bay region, California

Invasive species can have complex invasion histories, harbor cryptic levels of diversity, and pose taxonomic problems for pest management authorities. Roof rats, Rattus rattus sensu lato, are common invasive pests of the San Francisco Bay Area in California, USA. They are a significant health risk and pest management efforts impose a large financial investment from public institutions and private individuals. Recent molecular genetic and taxonomic studies of black rats in their native range in Asia have shown that the species is a complex of two karyotypic forms and four mitochondrial genetic lineages that may represent four distinct species. We used mtDNA sequences and nuclear microsatellite variation to identify which mitochondrial lineages of the R. rattus group are present in the San Francisco Bay Area and to test for gene flow among them. We recovered specimens with mtDNA sequences representing two of the major mtDNA lineages of the R. rattus group. Microsatellite variation, however, was not structured in concordance with mtDNA lineages, suggesting a more complex history involving hybridization and introgression between these lineages. Although Aplin et al. (2011) and Lack et al. (2012) reported R. rattus Lineage II in North America, this is the first detailed examination of possible gene flow amongst lineages in this region.

Phylogenetic Placement of the Pygmy Alligator Lizard Based on Mitochondrial DNA

Abstract Morphological studies have proven inconsistent in establishing the phylogenetic placement and taxonomic assignment of Elgaria parva. Originally classified as Gerrhonotus parvus Knight and Scudday, this taxon was reassigned to Elgaria based on morphology. To investigate its phylogenetic affinities, we generated mitochondrial DNA sequence data and conducted phylogenetic analyses together with published sequences for a broad taxonomic sampling of anguid lizards. We conducted parsimony, likelihood, and Bayesian analyses of the data. Our results indicate that E. parva forms a clade with other Gerrhonotus rather than Elgaria. Furthermore, Elgaria and Gerrhonotus are not sister taxa. Based on our new molecular evidence, we suggest that E. parva be classified as Gerrhonotus parvus as originally described.

Phylogeography of the western jumping mouse (Zapus princeps) detects deep and persistent allopatry with expansion

Abstract Understanding how diversity is partitioned across the landscape provides perspectives on the environmental processes that have influenced the evolutionary history of organisms. We analyzed spatial demography, historical biogeography, and niche divergence of the western jumping mouse (Zapus princeps) using molecular sequence data from mitochondrial and nuclear DNA recovered from 7 of the 11 subspecies in western North America. Phylogeographic structure within Z. princeps was partitioned across 5 clades (Boreal, Northern Sierra, Southern Rockies, Southern Sierra, and Uinta). Two lineages detected in the Sierra Nevada of California (Northern Sierra and Southern Sierra) were more closely allied to Z. trinotatus than to other lineages of Z. princeps and species distribution models mirror these phylogenetic signatures by detecting wide overlap in niches for Sierran jumping mice and Z. trinotatus as compared to other Z. princeps. Four southern lineages are deeply divergent and limited to disjunct mesic and montane habitats within the xeric southwestern United States, whereas the 5th lineage is widespread, extending from Wyoming to Alaska and reflecting expansion northward following deglaciation, a common pattern in boreal mammals.

NEW RECORDS OF SOREX PREBLEI AND S. TENELLUS IN CALIFORNIA

Abstract We identified 13 specimens of Prebles shrew (Sorex preblei) and 5 specimens of the Inyo shrew (Sorex tenellus) from Lassen Volcanic National Park (LVNP), California. These records represent the first captures of either species from LVNP and substantially extend the ranges of both. This is the first recorded instance of these 2 species occurring in sympatry.

Conservation genomics of desert dwelling California voles (Microtus californicus) and implications for management of endangered Amargosa voles (Microtus californicus scirpensis)

Understanding population genetic structure and levels of genetic variation is critical for the conservation and management of imperiled populations, especially when reintroductions are planned. We used restriction-site associated DNA (RAD) sequencing to study the genetic diversity and evolutionary relationships of the endangered Amargosa vole and other closely related desert-dwelling California voles. Specifically, we sought to determine how Amargosa voles are related to other California voles, how genetic variation is partitioned among subpopulations in wild Amargosa voles, and how much genetic variation is captured within a captive insurance colony of Amargosa voles. Our multilocus nuclear dataset provides strong evidence that Amargosa voles are part of a northern clade of California voles. Amargosa voles have highly reduced genetic variation relative to other California voles, but do exhibit some sub-structure among sampled marshes. Captive Amargosa voles capture approximately half of the total genetic variation present in the wild Amargosa vole populations. We discuss the management implications of our findings in light of reintroductions planned for Amargosa voles. Our study highlights the utility of reduced representation genomic approaches, like RADseq, to resolve relationships among small populations that are difficult to study with traditional markers due to low genetic variation and few individuals left in the wild.