Extraordinary levels of per- and polyfluoroalkyl substances (PFAS) in vertebrate animals at a New Mexico desert oasis: Multiple pathways for wildlife and human exposure.

Per- and polyfluoroalkyl substances (PFAS) in the environment pose persistent and complex threats to human and wildlife health. Around the world, PFAS point sources such as military bases expose thousands of populations of wildlife and game species, with potentially far-reaching implications for population and ecosystem health. But few studies shed light on the extent to which PFAS permeate food webs, particularly ecologically and taxonomically diverse communities of primary and secondary consumers. Here we conducted >2000 assays to measure tissue-concentrations of 17 PFAS in 23 species of mammals and migratory birds at Holloman Air Force Base (AFB), New Mexico, USA, where wastewater catchment lakes form biodiverse oases. PFAS concentrations were among the highest reported in animal tissues, and high levels have persisted for at least three decades. Twenty of 23 species sampled at Holloman AFB were heavily contaminated, representing middle trophic levels and wetland to desert microhabitats, implicating pathways for PFAS uptake: ingestion of surface water, sediments, and soil; foraging on aquatic invertebrates and plants; and preying upon birds or mammals. The hazardous long carbon-chain form, perfluorooctanosulfonic acid (PFOS), was most abundant, with liver concentrations averaging >10,000 ng/g wet weight (ww) in birds and mammals, respectively, and reaching as high 97,000 ng/g ww in a 1994 specimen. Perfluorohexanesulfonic acid (PFHxS) averaged thousands of ng/g ww in the livers of aquatic birds and littoral-zone house mice, but one order of magnitude lower in the livers of upland desert rodent species. Piscivores and upland desert songbirds were relatively uncontaminated. At control sites, PFAS levels were strikingly lower on average and different in composition. In sum, legacy PFAS at this desert oasis have permeated local aquatic and terrestrial food webs across decades, severely contaminating populations of resident and migrant animals, and exposing people via game meat consumption and outdoor recreation.

The genetic legacy of 50 years of desert bighorn sheep translocations.

Conservation biologists have increasingly used translocations to mitigate population declines and restore locally extirpated populations. Genetic data can guide the selection of source populations for translocations and help evaluate restoration success. Bighorn sheep (Ovis canadensis) are a managed big game species that suffered widespread population extirpations across western North America throughout the early 1900s. Subsequent translocation programs have successfully re-established many formally extirpated bighorn herds, but most of these programs pre-date genetically informed management practices. The state of Nevada presents a particularly well-documented case of decline followed by restoration of extirpated herds. Desert bighorn sheep (O. c. nelsoni) populations declined to less than 3,000 individuals restricted to remnant herds in the Mojave Desert and a few locations in the Great Basin Desert. Beginning in 1968, the Nevada Department of Wildlife translocated ~2,000 individuals from remnant populations to restore previously extirpated areas, possibly establishing herds with mixed ancestries. Here, we examined genetic diversity and structure among remnant herds and the genetic consequences of translocation from these herds using a genotyping-by-sequencing approach to genotype 17,095 loci in 303 desert bighorn sheep. We found a signal of population genetic structure among remnant Mojave Desert populations, even across geographically proximate mountain ranges. Further, we found evidence of a genetically distinct, potential relict herd from a previously hypothesized Great Basin lineage of desert bighorn sheep. The genetic structure of source herds was clearly reflected in translocated populations. In most cases, herds retained genetic evidence of multiple translocation events and subsequent admixture when founded from multiple remnant source herds. Our results add to a growing literature on how population genomic data can be used to guide and monitor restoration programs.

Integrative species delimitation of the widespread North American jumping mice (Zapodinae).

Delimiting species can be challenging, but is a key step for the critical examination of evolutionary history and for prioritizing conservation efforts. Because systematic relationships are often determined iteratively using tests based on taxonomy, such methods can fail to detect cryptic variation and result in biased conclusions. Conversely, discovery-based approaches provide a powerful way to define operational taxonomic units and test species boundaries. We compare both approaches (taxonomy-based delimitation - TBD and discovery-based delimitation - DBD) within North American jumping mice (Zapodinae) using broad sampling, multilocus analyses, and ecological tests. This group diversified through the dynamic glacial-interglacial periods of the Quaternary and phylogeographic tests reveal 28 lineages that correspond poorly with current taxonomy (4 species, 32 nominal subspecies). However, neither the 4-species or 28-lineage hypotheses are optimal for species-level classification. Rather, information theoretic approaches (Bayes Factors) indicate a 15-species hypothesis is best for characterizing genetic variation in this group, with subsequent iterative pairwise ecological tests failing to confirm four species pairs. Taken together, evolutionary and ecological tests capture divergence among 11 putative species that, if upheld by additional tests, will lead to taxonomic revision and reevaluation of conservation plans.

Revision of widespread red squirrels (genus: Tamiasciurus) highlights the complexity of speciation within North American forests.

Integration of molecular methods, ecological modeling, and statistical hypothesis testing are increasing our understanding of differentiation within species and phylogenetic relationships among species by revealing environmental connections to evolutionary processes. Within mammals, novel diversity is being discovered and characterized as more complete geographic sampling is coupled with newer multi-disciplinary approaches. North American red squirrels exemplify a forest obligate genus whose species are monitored as indicators of forest ecosystem condition, yet phylogenetic relationships reflecting evolutionary history within this genus remain tentative. Through testing of competing systematic and niche-based divergence hypotheses, we recognize three species, Tamiasciurus douglasii, T. hudsonicus, and T. fremonti. Our data provide evidence of regional differences in evolutionary dynamics and continental gradients of complexity that are important both for future management and for investigating multiple pathways that can lead to the formation of new species.

Accounting for rate variation among lineages in comparative demographic analyses.

Genetic analyses of contemporary populations can be used to estimate the demographic histories of species within an ecological community. Comparison of these demographic histories can shed light on community responses to past climatic events. However, species experience different rates of molecular evolution, and this presents a major obstacle to comparative demographic analyses. We address this problem by using a Bayesian relaxed-clock method to estimate the relative evolutionary rates of 22 small mammal taxa distributed across northwestern North America. We found that estimates of the relative molecular substitution rate for each taxon were consistent across the range of sampling schemes that we compared. Using three different reference rates, we rescaled the relative rates so that they could be used to estimate absolute evolutionary timescales. Accounting for rate variation among taxa led to temporal shifts in our skyline-plot estimates of demographic history, highlighting both uniform and idiosyncratic evolutionary responses to directional climate trends for distinct ecological subsets of the small mammal community. Our approach can be used in evolutionary analyses of populations from multiple species, including comparative demographic studies.

Using biogeographical history to inform conservation: the case of Preble's meadow jumping mouse.

The last Pleistocene deglaciation shaped temperate and boreal communities in North America. Rapid northward expansion into high latitudes created distinctive spatial genetic patterns within species that include closely related groups of populations that are now widely spread across latitudes, while longitudinally adjacent populations, especially those near the southern periphery, often are distinctive due to long-term disjunction. Across a spatial expanse that includes both recently colonized and long-occupied regions, we analysed molecular variation in zapodid rodents to explore how past climate shifts influenced diversification in this group. By combining molecular analyses with species distribution modelling and tests of ecological interchangeability, we show that the lineage including the Preble's meadow jumping mouse (Zapus hudsonius preblei), a US federally listed taxon of conservation concern, is not restricted to the southern Rocky Mountains. Rather, populations along the Front Range are part of a single lineage that is ecologically indistinct and extends to the far north. Of the 21 lineages identified, this Northern lineage has the largest geographical range and low measures of intralineage genetic differentiation, consistent with recent northward expansion. Comprehensive sampling combined with coalescent-based analyses and niche modelling leads to a radically different view of geographical structure within jumping mice and indicates the need to re-evaluate their taxonomy and management. This analysis highlights a premise in conservation biology that biogeographical history should play a central role in establishing conservation priorities.

Characterization of the rabbit agouti signaling protein (ASIP) gene: transcripts and phylogenetic analyses and identification of the causative mutation of the nonagouti black coat colour.

The agouti locus encodes the agouti signalling protein (ASIP) which is involved in determining the switch from eumelanin to pheomelanin synthesis in melanocytes. In the domestic rabbit (Oryctolagus cuniculus) early studies indicated three alleles at this locus: A, light-bellied agouti (wild type); a(t), black and tan; a, black nonagouti. We characterized the rabbit ASIP gene and identified the causative mutation (an insertion in exon 2) of the black nonagouti allele whose frequency was evaluated in 31 breeds. Phylogenetic analysis of ASIP sequences from Oryctolagus and 9 other species of the family Leporidae placed Oryctolagus as sister species to Pentalagus and Bunolagus. Transcription analysis in wild type agouti rabbits revealed the presence of two major transcripts with different 5'-untranslated regions having ventral or dorsal skin specific expression. ASIP gene transcripts were also detected in all examined rabbit tissues distinguishing the rabbit expression pattern from what was observed in wild type mice.