A community genomics approach to natural hybridization.

Hybridization is a complicated, oft-misunderstood process. Once deemed unnatural and uncommon, hybridization is now recognized as ubiquitous among species. But hybridization rates within and among communities are poorly understood despite the relevance to ecology, evolution and conservation. To clarify, we examined hybridization across 75 freshwater fish communities within the Ozarks of the North American Interior Highlands (USA) by single nucleotide polymorphism (SNP) genotyping 33 species (N = 2865 individuals; double-digest restriction site-associated DNA sequencing (ddRAD)). We found evidence of hybridization (70 putative hybrids; 2.4% of individuals) among 18 species-pairs involving 73% (24/33) of study species, with the majority being concentrated within one family (Leuciscidae/minnows; 15 species; 66 hybrids). Interspecific genetic exchange-or introgression-was evident from 24 backcrossed individuals (10/18 species-pairs). Hybrids occurred within 42 of 75 communities (56%). Four selected environmental variables (species richness, protected area extent, precipitation (May and annually)) exhibited 73-78% accuracy in predicting hybrid occurrence via random forest classification. Our community-level assessment identified hybridization as spatially widespread and environmentally dependent (albeit predominantly within one diverse, omnipresent family). Our approach provides a more holistic survey of natural hybridization by testing a wide range of species-pairs, thus contrasting with more conventional evaluations.

Riverscape community genomics: A comparative analytical approach to identify common drivers of spatial structure.

Genetic differentiation among local groups of individuals, that is, genetic ß-diversity, is a key component of population persistence related to connectivity and isolation. However, most genetic investigations of natural populations focus on a single species, overlooking opportunities for multispecies conservation plans to benefit entire communities in an ecosystem. We present an approach to evaluate genetic ß-diversity within and among many species and demonstrate how this riverscape community genomics approach can be applied to identify common drivers of genetic structure. Our study evaluated genetic ß-diversity in 31 co-distributed native stream fishes sampled from 75 sites across the White River Basin (Ozarks, USA) using SNP genotyping (ddRAD). Despite variance among species in the degree of genetic divergence, general spatial patterns were identified corresponding to river network architecture. Most species (N = 24) were partitioned into discrete subpopulations (K = 2-7). We used partial redundancy analysis to compare species-specific genetic ß-diversity across four models of genetic structure: Isolation by distance (IBD), isolation by barrier (IBB), isolation by stream hierarchy (IBH), and isolation by environment (IBE). A significant proportion of intraspecific genetic variation was explained by IBH (x̄ = 62%), with the remaining models generally redundant. We found evidence for consistent spatial modularity in that gene flow is higher within rather than between hierarchical units (i.e., catchments, watersheds, basins), supporting the generalization of the stream hierarchy model. We discuss our conclusions regarding conservation and management and identify the 8-digit hydrologic unit (HUC) as the most relevant spatial scale for managing genetic diversity across riverine networks.

A needle in the haystack? Applying species co-occurrence frameworks with fish assemblage data to identify species associations and sharpen ecological hypotheses.

Different species can associate or interact in many ways, and methods exist for inferring associations and underlying mechanisms from incidence data (e.g., co-occurrence frameworks). These methods have received criticism despite their recent resurgence in the literature. However, co-occurrence frameworks for identifying nonrandomly associated species pairs (e.g., aggregated or segregated pairs) have value as heuristic tools for sharpening hypotheses concerning fish ecology. This paper provides a case study examining species co-occurrence across 33 stream fish assemblages in southeastern Oklahoma, USA, which were sampled twice (1974 and 2014). This study sought to determine (a) which species were nonrandomly associated, (b) what processes might have driven these associations and (c) how consistent patterns were across time. Associations among most pairs of species (24 species, 276 unique pairs) were not significantly different from random (>80%). Among all significant, nonrandomly associated species pairs (54 unique pairs), 78% (42 pairs) were aggregated and 22% (12 pairs) segregated. Most of these (28 pairs, 52%) were hypothesized to be driven by nonbiotic mechanisms: habitat filtering (20 pairs, 37%), dispersal limitation (two pairs, 0.4%) or both (six pairs, 11%). The remaining 26 nonrandomly associated pairs (48%) had no detectable signal of spatial or environmental factors involved with the association, therefore the potential for biotic interaction was not refuted. Only five species pairs were consistently associated across both sampling periods: stonerollers Campostoma spp. and orangebelly darter Etheostoma radiosum; red shiner Cyprinella lutrensis and bullhead minnow Pimephales vigilax; bluegill sunfish Lepomis macrochirus and redear sunfish Lepomis microlophus; redfin shiner Lythrurus umbratilis and bluntnose minnow Pimephales notatus; and bigeye shiner Notropis boops and golden shiner Notemigonus crysoleucas. Frameworks for identifying nonrandomly associated species pairs can provide insight into broader mechanisms of species assembly and point to potentially interesting species interactions (out of many possible pairs). However, this approach is best applied as a tool for sharpening hypotheses to be investigated further. Rather than a weakness, the heuristic nature is the strength of such methods, and can help guide biologists toward better questions by employing relatively cheap diversity survey data, which are often already in hand, to reduce complex interaction networks down to their nonstochastic parts which warrant further investigation.

The Himalayan uplift and evolution of aquatic biodiversity across Asia: Snowtrout (Cyprininae: Schizothorax) as a test case.

Global biodiversity hotspots are often remote, tectonically active areas undergoing climatic fluctuations, such as the Himalaya Mountains and neighboring Qinghai-Tibetan Plateau (QTP). They provide biogeographic templates upon which endemic biodiversity can be mapped to infer diversification scenarios. Yet, this process can be somewhat opaque for the Himalaya, given substantial data gaps separating eastern and western regions. To help clarify, we evaluated phylogeographic and phylogenetic hypotheses for a widespread fish (Snowtrout: Cyprininae; Schizothorax) by sequencing 1,140 base pair of mtDNA cytochrome-b (cytb) from Central Himalaya samples (Nepal: N = 53; Bhutan: N = 19), augmented with 68 GenBank sequences (N = 60 Schizothorax/N = 8 outgroups). Genealogical relationships (N = 132) were analyzed via maximum likelihood (ML), Bayesian (BA), and haplotype network clustering, with clade divergence estimated via TimeTree. Snowtrout seemingly originated in Central Asia, dispersed across the QTP, then into Bhutan via southward-flowing tributaries of the east-flowing Yarlung-Tsangpo River (YLTR). Headwaters of five large Asian rivers provided dispersal corridors from Central into eastern/southeastern Asia. South of the Himalaya, the YLTR transitions into the Brahmaputra River, facilitating successive westward colonization of Himalayan drainages first in Bhutan, then Nepal, followed by far-western drainages subsequently captured by the (now) westward-flowing Indus River. Two distinct Bhutanese phylogenetic groups were recovered: Bhutan-1 (with three subclades) seemingly represents southward dispersal from the QTP; Bhutan-2 apparently illustrates northward colonization from the Lower Brahmaputra. The close phylogenetic/phylogeographic relationships between the Indus River (Pakistan) and western tributaries of the Upper Ganges (India/Nepal) potentially implicate an historic, now disjunct connection. Greater species-divergences occurred across rather than within-basins, suggesting vicariance as a driver. The Himalaya is a component of the Earth's largest glacial reservoir (i.e., the "third-pole") separate from the Arctic/Antarctic. Its unique aquatic biodiversity must be defined and conserved through broad, trans-national collaborations. Our study provides an initial baseline for this process.

Spatial population genetics in heavily managed species: Separating patterns of historical translocation from contemporary gene flow in white-tailed deer.

Approximately 100 years ago, unregulated harvest nearly eliminated white-tailed deer (Odocoileus virginianus) from eastern North America, which subsequently served to catalyze wildlife management as a national priority. An extensive stock-replenishment effort soon followed, with deer broadly translocated among states as a means of re-establishment. However, an unintended consequence was that natural patterns of gene flow became obscured and pretranslocation signatures of population structure were replaced. We applied cutting-edge molecular and biogeographic tools to disentangle genetic signatures of historical management from those reflecting spatially heterogeneous dispersal by evaluating 35,099 single nucleotide polymorphisms (SNPs) derived via reduced-representation genomic sequencing from 1143 deer sampled statewide in Arkansas. We then employed Simpson's diversity index to summarize ancestry assignments and visualize spatial genetic transitions. Using sub-sampled transects across these transitions, we tested clinal patterns across loci against theoretical expectations of their response under scenarios of re-colonization and restricted dispersal. Two salient results emerged: (A) Genetic signatures from historic translocations are demonstrably apparent; and (B) Geographic filters (major rivers; urban centers; highways) now act as inflection points for the distribution of this contemporary ancestry. These results yielded a statewide assessment of contemporary population structure in deer as driven by historic translocations as well as ongoing processes. In addition, the analytical framework employed herein to effectively decipher extant/historic drivers of deer distribution in Arkansas is also applicable for other biodiversity elements with similarly complex demographic histories.

Temporal dynamics of stream fish assemblages and the role of spatial scale in quantifying change.

Spatial grain of studies of communities is often based on arbitrary convention. Few studies have examined how spatial scaling of grain size affects estimates of compositional change over time, despite its broad implications.Fish assemblage structure was compared between 1974 and 2014 at 33 sampling locations in the Muddy Boggy River drainage, USA. The two main objectives for this comparison were to quantify change in assemblage structure and to test for a relationship between compositional change and spatial scale. Spatial scale was manipulated by pooling assemblage data into a continuous range of groups, which increased in size from K = 33 pairs (i.e., local scale) to K = 1 pair (i.e., global scale), via clustering algorithm based on pair-wise fluvial distance.Local assemblages (stream reaches) varied in the degree of assemblage change over time (range = 0.10-0.99 dissimilarity; mean = 0.66). The global assemblage (drainage), however, remained relatively similar. A discontinuity in the relationship between compositional change and spatial scale occurred at K = 15 (mean dissimilarity = 0.56; p = .062), and this grouping is roughly the size of the headwater/tributary drainages (i.e., stream order ≤ 3) in the study system.Spatial scale can impact estimates of biodiversity change over time. These results suggest assemblages are more dynamic at individual stream reaches than at the scale of the entire drainage. The decline in assemblage change at the spatial scale of K = 15 deserves further attention given the marginal significance, despite a small sample size (n = 15). This pattern could suggest regional and meta-community processes become more important in shaping assemblage dynamics at the scale of headwater drainages, whereas the factors responsible for driving individual stream reach dynamics (e.g., stochasticity) become less important. Defining assemblages at a larger scale will result in different estimates of species persistence. Biodiversity monitoring efforts must take the effect of spatial scaling into consideration.

Age structuring and spatial heterogeneity in prion protein gene (PRNP) polymorphism in white-tailed deer.

Chronic-wasting disease (CWD) is a prion-derived fatal neurodegenerative disease that has affected wild cervid populations on a global scale. Susceptibility has been linked unambiguously to several amino acid variants within the prion protein gene (PRNP). Quantifying their distribution across landscapes can provide critical information for agencies attempting to adaptively manage CWD. Here we attempt to further define management implications of PRNP polymorphism by quantifying the contemporary geographic distribution (i.e., phylogeography) of PRNP variants in hunter-harvested white-tailed deer (WTD; Odocoileus virginianus, N = 1433) distributed across Arkansas (USA), including a focal spot for CWD since detection of the disease in February 2016. Of these, PRNP variants associated with the well-characterized 96S non-synonymous substitution showed a significant increase in relative frequency among older CWD-positive cohorts. We interpreted this pattern as reflective of a longer life expectancy for 96S genotypes in a CWD-endemic region, suggesting either decreased probabilities of infection or reduced disease progression. Other variants showing statistical signatures of potential increased susceptibility, however, seemingly reflect an artefact of population structure. We also showed marked heterogeneity across the landscape in the prevalence of 'reduced susceptibility' genotypes. This may indicate, in turn, that differences in disease susceptibility among WTD in Arkansas are an innate, population-level characteristic that is detectable through phylogeographic analysis.