Emily K. Latch

Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation

Traditional methods for characterizing genetic differentiation among populations rely on a priori grouping of individuals. Bayesian clustering methods avoid this limitation by using linkage and Hardy–Weinberg disequilibrium to decompose a sample of individuals into genetically distinct groups. There are several software programs available for Bayesian clustering analyses, all of which describe a decrease in the ability to detect distinct clusters as levels of genetic differentiation among populations decrease. However, no study has yet compared the performance of such methods at low levels of population differentiation, which may be common in species where populations have experienced recent separation or high levels of gene flow. We used simulated data to evaluate the performance of three Bayesian clustering software programs, PARTITION, STRUCTURE, and BAPS, at levels of population differentiation below FST=0.1. PARTITION was unable to correctly identify the number of subpopulations until levels of FST reached around 0.09. Both STRUCTURE and BAPS performed very well at low levels of population differentiation, and were able to correctly identify the number of subpopulations at FST around 0.03. The average proportion of an individual’s genome assigned to its true population of origin increased with increasing FST for both programs, reaching over 92% at an FST of 0.05. The average number of misassignments (assignments to the incorrect subpopulation) continued to decrease as FST increased, and when FST was 0.05, fewer than 3% of individuals were misassigned using either program. Both STRUCTURE and BAPS worked extremely well for inferring the number of clusters when clusters were not well-differentiated (FST=0.02–0.03), but our results suggest that FST must be at least 0.05 to reach an assignment accuracy of greater than 97%.

Species‐wide phylogeography of North American mule deer (Odocoileus hemionus): cryptic glacial refugia and postglacial recolonization

Quaternary climatic oscillations greatly influenced the present‐day population genetic structure of animals and plants. For species with high dispersal and reproductive potential, phylogeographic patterns resulting from historical processes can be cryptic, overshadowed by contemporary processes. Here we report a study of the phylogeography of Odocoileus hemionus, a large, vagile ungulate common throughout western North America. We examined sequence variation of mitochondrial DNA (control region and cytochrome b) within and among 70 natural populations across the entire range of the species. Among the 1766 individual animals surveyed, we recovered 496 haplotypes. Although fine‐scale phylogenetic structure was weakly resolved using phylogenetic methods, network analysis clearly revealed the presence of 12 distinct haplogroups. The spatial distribution of haplogroups showed a strong genetic discontinuity between the two morphological types of O. hemionus, mule deer and black‐tailed deer, east and west of the Cascade Mountains in the Pacific Northwest. Within the mule deer lineage, we identified several haplogroups that expanded before or during the Last Glacial Maximum, suggesting that mule deer persisted in multiple refugia south of the ice sheets. Patterns of genetic diversity within the black‐tailed deer lineage suggest a single refugium along the Pacific Northwest coast, and refute the hypothesis that black‐tailed deer persisted in one or more northern refugia. Our data suggest that black‐tailed deer recolonized areas in accordance with the pattern of glacial retreat, with initial recolonization northward along a coastal route and secondary recolonization inland.

Deciphering Ecological Barriers to North American River Otter (Lontra canadensis) Gene Flow in the Louisiana Landscape

For North American river otters (Lontra canadensis) in Louisiana, statewide distribution, availability of aquatic habitats, and the absence of physical barriers to dispersal might suggest that they exist as a large, panmictic population. However, the wide variety of habitat types in this region, and the dynamic nature of these habitats over time, could potentially structure river otter populations in accordance with cryptic landscape features. Recently developed landscape genetic models offer a spatially explicit approach that could be useful in identifying potential barriers to the movement of river otters through the dynamic aquatic landscape of Louisiana. We used georeferenced multilocus microsatellite genotypes in spatially implicit (STRUCTURE) and spatially explicit (GENELAND) models to characterize patterns of landscape genetic structure. All models identified 3 subpopulations of river otters in Louisiana, corresponding to Inland, Atchafalaya River, and Mississippi River regions. Variation in breeding seasonality, brought about by variation in prey abundance between inland and coastal populations, may have contributed to genetic differentiation among populations. It is also possible that the genetic discontinuities we observed indicate a correlation between otter distribution and access to freshwater. Regardless of the mechanism, it is likely that any genetic differentiation among subpopulations is exacerbated by relatively poor dispersal.

The effects of gene flow and population isolation on the genetic structure of␣reintroduced wild turkey populations: Are genetic signatures of source populations retained?

To counter losses of genetic diversity in reintroduced populations, species sometimes are reintroduced into networks of populations with the potential to exchange individuals. In reintroduced populations connected by gene flow, patterns of genetic structure initiated by the founding event may become obscured, and populations may eventually follow an isolation-by-distance model of genetic differentiation. Taking advantage of well-documented reintroduction histories of wild turkey populations in Indiana, we assessed the degree to which gene flow among reintroduced populations has obscured genetic signatures left by the founding events. Using a suite of nuclear microsatellite loci and sequence data from the mitochondrial control region, we characterized the level of genetic diversity and degree of genetic structure within and among: (1) reintroduced populations in isolated northern Indiana Fish and Wildlife Areas, (2) reintroduced populations in southern Indiana Fish and Wildlife Areas, where the distribution of populations is more continuous, and (3) source populations used for these reintroductions. We also utilized individual-based assignment tests to determine the relative contribution of source populations to the current distribution of alleles in reintroduced populations. Our results indicate that wild turkey reintroductions in Indiana have left distinct genetic signatures on populations that are detectable even after several decades. Although we found some case-specific evidence for gene flow, particularly in regions where populations are in close proximity, our data indicate on overall paucity of gene flow at a regional scale. Such post-reintroduction genetic monitoring has immediate implications for the design of optimal strategies to reintroduce wildlife for conservation and management.

Assessing Hybridization in Wildlife Populations Using Molecular Markers: A Case Study in Wild Turkeys

Abstract Extensive translocation of wildlife throughout North America has led to concerns regarding taxonomic integrity for a number of species. Often, multiple subspecies or variants were translocated into a common habitat or region, creating the opportunity for hybridization to occur. This issue is of particular concern to managers of wild turkeys (Meleagris gallopavo), a species in which considerable mixing of subspecies has occurred. We aim to quantify the subspecific status and degree of hybridization of individuals within an introduced population of Merriams turkeys (M. g. merriami) in the Davis Mountains of Texas, USA, and within nearby Rio Grande turkey populations (M. g. intermedia). We used data from the Merriams source population in New Mexico, USA, as a baseline reference for the genetic characteristics of the Merriams subspecies. Nineteen years following the introduction event, microsatellite data indicate that the genetic integrity of the introduced population of Merriams turkeys in the Davis Mountains Preserve has been eroded by both immigration from and hybridization with nearby Rio Grande populations. Data from the mitochondrial control region allow for further characterization of hybrid individuals and indicate that most hybrids were the result of immigrant Rio Grande males mating with resident Merriams females. Our results attribute to the potential importance of hybridization in wildlife species and suggest that hybridization can be a rapid process capable of drastically altering the evolutionary integrity of animals in a region.

Performance of partial statistics in individual-based landscape genetics

Individual‐based landscape genetic methods have become increasingly popular for quantifying fine‐scale landscape influences on gene flow. One complication for individual‐based methods is that gene flow and landscape variables are often correlated with geography. Partial statistics, particularly Mantel tests, are often employed to control for these inherent correlations by removing the effects of geography while simultaneously correlating measures of genetic differentiation and landscape variables of interest. Concerns about the reliability of Mantel tests prompted this study, in which we use simulated landscapes to evaluate the performance of partial Mantel tests and two ordination methods, distance‐based redundancy analysis (dbRDA) and redundancy analysis (RDA), for detecting isolation by distance (IBD) and isolation by landscape resistance (IBR). Specifically, we described the effects of suitable habitat amount, fragmentation and resistance strength on metrics of accuracy (frequency of correct results, type I/II errors and strength of IBR according to underlying landscape and resistance strength) for each test using realistic individual‐based gene flow simulations. Mantel tests were very effective for detecting IBD, but exhibited higher error rates when detecting IBR. Ordination methods were overall more accurate in detecting IBR, but had high type I errors compared to partial Mantel tests. Thus, no one test outperformed another completely. A combination of statistical tests, for example partial Mantel tests to detect IBD paired with appropriate ordination techniques for IBR detection, provides the best characterization of fine‐scale landscape genetic structure. Realistic simulations of empirical data sets will further increase power to distinguish among putative mechanisms of differentiation.

Identification of Novel Single Nucleotide Polymorphisms (SNPs) in Deer (Odocoileus spp.) Using the BovineSNP50 BeadChip

Single nucleotide polymorphisms (SNPs) are growing in popularity as a genetic marker for investigating evolutionary processes. A panel of SNPs is often developed by comparing large quantities of DNA sequence data across multiple individuals to identify polymorphic sites. For non-model species, this is particularly difficult, as performing the necessary large-scale genomic sequencing often exceeds the resources available for the project. In this study, we trial the Bovine SNP50 BeadChip developed in cattle (Bos taurus) for identifying polymorphic SNPs in cervids Odocoileus hemionus (mule deer and black-tailed deer) and O. virginianus (white-tailed deer) in the Pacific Northwest. We found that 38.7% of loci could be genotyped, of which 5% (n = 1068) were polymorphic. Of these 1068 polymorphic SNPs, a mixture of putatively neutral loci (n = 878) and loci under selection (n = 190) were identified with the FST-outlier method. A range of population genetic analyses were implemented using these SNPs and a panel of 10 microsatellite loci. The three types of deer could readily be distinguished with both the SNP and microsatellite datasets. This study demonstrates that commercially developed SNP chips are a viable means of SNP discovery for non-model organisms, even when used between very distantly related species (the Bovidae and Cervidae families diverged some 25.1−30.1 million years before present).

Fine-Scale Analysis Reveals Cryptic Landscape Genetic Structure in Desert Tortoises

Characterizing the effects of landscape features on genetic variation is essential for understanding how landscapes shape patterns of gene flow and spatial genetic structure of populations. Most landscape genetics studies have focused on patterns of gene flow at a regional scale. However, the genetic structure of populations at a local scale may be influenced by a unique suite of landscape variables that have little bearing on connectivity patterns observed at broader spatial scales. We investigated fine-scale spatial patterns of genetic variation and gene flow in relation to features of the landscape in desert tortoise (Gopherus agassizii), using 859 tortoises genotyped at 16 microsatellite loci with associated data on geographic location, sex, elevation, slope, and soil type, and spatial relationship to putative barriers (power lines, roads). We used spatially explicit and non-explicit Bayesian clustering algorithms to partition the sample into discrete clusters, and characterize the relationships between genetic distance and ecological variables to identify factors with the greatest influence on gene flow at a local scale. Desert tortoises exhibit weak genetic structure at a local scale, and we identified two subpopulations across the study area. Although genetic differentiation between the subpopulations was low, our landscape genetic analysis identified both natural (slope) and anthropogenic (roads) landscape variables that have significantly influenced gene flow within this local population. We show that desert tortoise movements at a local scale are influenced by features of the landscape, and that these features are different than those that influence gene flow at larger scales. Our findings are important for desert tortoise conservation and management, particularly in light of recent translocation efforts in the region. More generally, our results indicate that recent landscape changes can affect gene flow at a local scale and that their effects can be detected almost immediately.

Evaluation of a remnant lake sturgeon population’s utility as a source for reintroductions in the Ohio River system

The selection of an appropriate source population may be crucial to the long-term success of reintroduction programs. Appropriate source populations often are those that originate from the same genetic lineage as native populations. However, source populations also should exhibit high levels of genetic diversity to maximize their capacity to adapt to variable environmental conditions. Finally, it is preferable if source populations are genetically representative of historical lineages with little or no contamination from non-native or domesticated stocks. Here, we use nuclear (microsatellite) and cytoplasmic (mitochondrial control region) markers to assess the genetic suitability of a potential source population inhabiting the White River in Indiana: the last extant lake sturgeon population in the Ohio River drainage. The White River population exhibited slightly lower levels of genetic diversity than other lake sturgeon populations. However, the population’s two private microsatellite alleles and three private haplotypes suggest a unique evolutionary trajectory. Population assignment tests revealed only two putative migrants in the White River, indicating the population has almost completely maintained its genetic integrity. Additionally, pairwise FST estimates indicated significant levels of genetic divergence between the White River and seven additional lake sturgeon populations, suggesting its genetic distinctiveness. These data indicate that the White River population may be the most suitable source population for future lake sturgeon reintroductions throughout the Ohio River drainage. Furthermore, the White River population appears to be a reservoir of unique genetic information and reintroduction may be a necessary strategy to ensure the persistence of this important genetic lineage.

Hybrid swarm between divergent lineages of mule deer (Odocoileus hemionus)

Studies of hybrid zones have revealed an array of evolutionary outcomes, yet the underlying structure is typically characterized as one of three types: a hybrid zone, a hybrid swarm or a hybrid taxon. Our primary objective was to determine which of these three structures best characterizes a zone of hybridization between two divergent lineages of mule deer (Odocoileus hemionus), mule deer and black‐tailed deer. These lineages are morphologically, ecologically and genetically distinct, yet hybridize readily along a zone of secondary contact between the east and west slopes of the Cascade Mountains (Washington and Oregon, USA). Using microsatellite and mitochondrial DNA, we found clear evidence for extensive hybridization and introgression between lineages, with varying degrees of admixture across the zone of contact. The pattern of hybridization in this region closely resembles a hybrid swarm; based on data from 10 microsatellite loci, we detected hybrids that extend well beyond the F1 generation, did not detect linkage disequilibrium at the centre of the zone and found that genotypes were associated randomly within the zone of contact. Introgression was characterized as bidirectional and symmetric, which is surprising given that the zone of contact occurs along a sharp ecotone and that lineages are characterized by large differences in body size (a key component of mating success). Regardless of the underlying mechanisms promoting hybrid swarm maintenance, it is clear that the persistence of a hybrid swarm presents unique challenges for management in this region.