Population structure of California coyotes corresponds to habitat-specific breaks and illuminates species history

Little is known about the relationship between animal movements and the emergent structure of populations, especially for species occupying large continuous distributions. Some such mammals disperse disproportionately into habitat similar to their natal habitat, a behavioural bias that might be expected to lead to habitat-conforming genetic structure. We hypothesized that coyotes (Canis latrans) would exhibit such natal-biased dispersal, and used 13 microsatellite loci to test, correspondingly, whether genetic structure conformed to major habitat breaks. First, we used a model-based approach to assign coyote genotypes to distinct genetic clusters irrespective of geographical location. Visualization on a geographical information system revealed a strong concordance between the locations of cluster assignments and habitat bioregions, not explainable in terms of physical dispersal barriers or intervening low-quality habitat. Next, we used a multiple Mantel test, which controlled for effects of geographical distance (itself, marginally significant; P = 0.06), to statistically determine that genetic distance was indeed higher between than within bioregions (P < 0.001). Whereas previously published examples of landscape effects on gene flow have typically been explainable in terms of species-wide habitat affinities or dispersal barriers, our finding that genetic subdivisions were associated with unobstructed boundaries between contiguous habitats suggests a role for intraspecific variability in habitat affinities as a factor underlying genetic structure. In addition, our data combined with previously published data suggest a pattern of genetic isolation-by-distance throughout western North America, consistent with independent evidence that the western half of the coyote range predates European settlement.     

Simultaneous detection of linkage disequilibrium and genetic differentiation of subdivided populations

We propose a new method for simultaneously detecting linkage disequilibrium and genetic structure in subdivided populations. Taking subpopulation structure into account with a hierarchical model, we estimate the magnitude of genetic differentiation and linkage disequilibrium in a metapopulation on the basis of geographical samples, rather than decompose a population into a finite number of random-mating subpopulations. We assume that Hardy-Weinberg equilibrium is satisfied in each locality, but do not assume independence between marker loci. Linkage states remain unknown. Genetic differentiation and linkage disequilibrium are expressed as hyperparameters describing the prior distribution of genotypes or haplotypes. We estimate related parameters by maximizing marginal-likelihood functions and detect linkage equilibrium or disequilibrium by the Akaike information criterion. Our empirical Bayesian model analyzes genotype and haplotype frequencies regardless of haploid or diploid data, so it can be applied to most commonly used genetic markers. The performance of our procedure is examined via numerical simulations in comparison with classical procedures. Finally, we analyze isozyme data of ayu, a severely exploited fish species, and single-nucleotide polymorphisms in human ALDH2.     

Comparative population structure and genetic diversity of Arceuthobium americanum (Viscaceae) and its Pinus host species: insight into host-parasite evolution in parasitic angiosperms

In a recent study we revealed that the parasitic angiosperm Arceuthobium americanum is comprised of three distinct genetic races, each associated with a different host in regions of allopatry. In order to assess the role of host identity and geographical isolation on race formation in A. americanum, we compared the genetic population structure of this parasite with that of its three principal hosts, Pinus banksiana, Pinus contorta var. latifolia and Pinus contorta var. murrayana. Despite the fact that A. americanum was divided into three genetic races, hosts were divided into only two genetic groups: (i) Pinus banksiana and hybrids, and (ii) P. contorta var. latifolia and var. murrayana. These findings suggest that factors such as geographical isolation and adaptation to different environmental conditions are important for race formation in the absence of host-driven selection pressures. To assess factors impacting population structure at the fine-scale, genetic and geographical distance matrices of host and parasite were compared within A. americanum races. The lack of a relationship between genetic and geographical distance matrices suggests that isolation-by-distance plays a negligible role at this level. The effect of geographical isolation may have been diminished because of the influence of factors such as random seed dispersal by animal vectors or adaptation to nongeographically patterned environmental conditions. Host-parasite interactions might also have impacted the fine-scale structure of A. americanum because the parasite and host were found to have similar patterns of gene flow.     

Tracing genetic differentiation of Chinese Mongolian sheep using microsatellites

The genetic consequences of population differentiation and isolation have been the subject of conservation biology. In this study, we analysed the genetic diversity and structure of Mongolian sheep in China. These animals belong to a traditional local breed with high production, extensive adaption, early maturity and roughage resistance. For this purpose, 26 microsatellites were genotyped for five Mongolian sheep populations. The Bayesian clustering indicated five clusters as the most probable genetic structure of the populations investigated. In addition, a clear genetic structure was revealed in three populations distributed at large geographical scales, while the other cluster encompassed UQ and HLBR sheep that displayed no clear differentiation, probably due to their close and small geographical distributions. Overall, our results are helpful in understanding the interplay of population dynamics in these close genetic lineages of Mongolian sheep.     

Ancient trade routes shaped the genetic structure of horses in eastern Eurasia

Animal exchange networks have been shown to play an important role in determining gene flow among domestic animal populations. The Silk Road is one of the oldest continuous exchange networks in human history, yet its effectiveness in facilitating animal exchange across large geographical distances and topographically challenging landscapes has never been explicitly studied. Horses are known to have been traded along the Silk Roads; however, extensive movement of horses in connection with other human activities may have obscured the genetic signature of the Silk Roads. To investigate the role of the Silk Roads in shaping the genetic structure of horses in eastern Eurasia, we analysed microsatellite genotyping data from 455 village horses sampled from 17 locations. Using least‐cost path methods, we compared the performance of models containing the Silk Roads as corridors for gene flow with models containing single landscape features. We also determined whether the recent isolation of former Soviet Union countries from the rest of Eurasia has affected the genetic structure of our samples. The overall level of genetic differentiation was low, consistent with historically high levels of gene flow across the study region. The spatial genetic structure was characterized by a significant, albeit weak, pattern of isolation by distance across the continent with no evidence for the presence of distinct genetic clusters. Incorporating landscape features considerably improved the fit of the data; however, when we controlled for geographical distance, only the correlation between genetic differentiation and the Silk Roads remained significant, supporting the effectiveness of this ancient trade network in facilitating gene flow across large geographical distances in a topographically complex landscape.     

Effects of Pleistocene climate changes on species ranges and evolutionary processes in the Neotropical Atlantic Forest

The effects of global glaciations on the distribution of organisms is an essential element of many diversification models. However, the empirical evidence supporting this idea is mixed, in particular with respect to explaining tropical forest evolution. In the present study, we evaluated the impacts of range shifts associated with Pleistocene global glacial cycles on the evolution of tropical forests. In particular, we tested the predictions: (1) that population genetic structure increases with fragmentation variation between the present and the Last Glacial Maximum (LGM) and also (2) with geographical range instability; and (3) that genetic diversity increases with range stability and (4) decreases with fragmentation variation between periods. To address our predictions, we studied population genetic structures and modelled present and past distributions of 15 Atlantic Forest (AF) endemic birds. Afterwards, we evaluated the relationship of population genetic parameters with metrics of species range shifts between the present and the LGM. We found that geographical ranges of AF birds changed in concert with Pleistocene glacial cycles but, unexpectedly, our findings suggest the novel idea that ranges during glacial maxima were slightly larger on average, as well as equally fragmented and displaced from the interglacial ranges. Our findings suggest that range shifts over the late Pleistocene impacted on the diversification of forest organisms, although they did not show that those range shifts had a strong effect. We found that a combination of fragmentation variation across time, small current range size, and range stability increased population genetic structure. However, neither fragmentation, nor range stability affected genetic diversity. Our study showed that evolutionary responses to range shifts across AF birds have a high variance, which could explain the mixed support given by single‐species studies to the action of Pleistocene range shifts on population evolution.     

Microsatellite variation among diverging populations of Drosophila mojavensis

Divergence and speciation may occur by various means, depending on the particular history, selective environments, and genetic composition of populations. In Drosophila mojavensis, a good model of incipient speciation, understanding the population genetic structure within this group facilitates our ability to understand the context in which reproductive isolation among populations is developing. Here we report the genetic structure and relationships of D. mojavensis populations at nuclear loci. We surveyed 29 populations throughout the distribution of D. mojavensis for four microsatellite loci to differentiation among populations of this species. These loci reveal four distinct geographical regions of D. mojavensis populations in the south-western United States and north-western Mexico--(i) Baja California peninsula (Baja), (ii) Sonora, Mexico-southern Arizona, United States (Sonora), (iii) Mojave Desert and Grand Canyon (Mojave), and (iv) Santa Catalina Island (Catalina). While all regions show strong isolation, Mojave and Catalina are highly diverged from other regions. Within any region, populations are largely homogenous over broad geographical distances. Based on the population structure, we find clear geographical barriers to gene flow appear to have a strong effect in isolating populations across regions for this species.     

Spatial autocorrelation of allozyme and quantitative markers within a natural population of Centaurea jacea (Asteraceae)

This paper compares the fine‐scale genetic structure of quantitative traits and allozyme markers within a natural population of Centaurea jacea s.l. To that end, a spatial autocorrelation approach is developed based on pairwise correlation coefficients between individuals and using sib families. Statistical properties of the proposed statistics are investigated with numerical simulations. Our results show that most quantitative traits have a significant spatial structure for their genetic component. On average, allozyme markers and the genetic component of quantitative traits have similar patterns of spatial autocorrelation that are consistent with a neutral model of isolation by distance. We also show evidence that environmental heterogeneity generates a spatial structure for the environmental component of quantitative traits. Results are discussed in terms of mechanisms generating spatial structure and are compared with those obtained on a large geographical scale.     

Continent-Wide Decoupling of Y-Chromosomal Genetic Variation from Language and Geography in Native South Americans

Numerous studies of human populations in Europe and Asia have revealed a concordance between their extant genetic structure and the prevailing regional pattern of geography and language. For native South Americans, however, such evidence has been lacking so far. Therefore, we examined the relationship between Y-chromosomal genotype on the one hand, and male geographic origin and linguistic affiliation on the other, in the largest study of South American natives to date in terms of sampled individuals and populations. A total of 1,011 individuals, representing 50 tribal populations from 81 settlements, were genotyped for up to 17 short tandem repeat (STR) markers and 16 single nucleotide polymorphisms (Y-SNPs), the latter resolving phylogenetic lineages Q and C. Virtually no structure became apparent for the extant Y-chromosomal genetic variation of South American males that could sensibly be related to their inter-tribal geographic and linguistic relationships. This continent-wide decoupling is consistent with a rapid peopling of the continent followed by long periods of isolation in small groups. Furthermore, for the first time, we identified a distinct geographical cluster of Y-SNP lineages C-M217 (C3*) in South America. Such haplotypes are virtually absent from North and Central America, but occur at high frequency in Asia. Together with the locally confined Y-STR autocorrelation observed in our study as a whole, the available data therefore suggest a late introduction of C3* into South America no more than 6,000 years ago, perhaps via coastal or trans-Pacific routes. Extensive simulations revealed that the observed lack of haplogroup C3* among extant North and Central American natives is only compatible with low levels of migration between the ancestor populations of C3* carriers and non-carriers. In summary, our data highlight the fact that a pronounced correlation between genetic and geographic/cultural structure can only be expected under very specific conditions, most of which are likely not to have been met by the ancestors of native South Americans.     

Geographical barriers and climate influence demographic history in narrowleaf cottonwoods

Studies of genetic variation can clarify the role of geography and spatio-temporal variation of climate in shaping demography, particularly in temperate zone tree species with large latitudinal ranges. Here, we examined genetic variation in narrowleaf cottonwood, Populus angustifolia, a dominant riparian tree. Using multi-locus surveys of polymorphism in 363 individuals across the species'' 1800 km latitudinal range, we found that, first, P. angustifolia has stronger neutral genetic structure than many forest trees (simple sequence repeat (SSR) F_ST=0.21), with major genetic groups corresponding to large apparent geographical barriers to gene flow. Second, using SSRs and putatively neutral sequenced loci, coalescent simulations indicated that populations diverged before the last glacial maximum (LGM), suggesting the presence of population structure before the LGM. Third, the LGM and subsequent warming appear to have had different influences on each of these distinct populations, with effective population size reduction in the southern extent of the range but major expansion in the north. These results are consistent with the hypothesis that climate and geographic barriers have jointly affected the demographic history of P. angustifolia, and point the importance of both factors as being instrumental in shaping genetic variation and structure in widespread forest trees.     

A geographical genetics framework for inferring homing reproductive behavior in fishes

One of the most intriguing patterns of migration and gene flow that affects genetic structure is the reproductive homing behavior of fishes, wherein the adults return to the areas in which they were spawned. Here we reviewed the literature on homing behavior in fish and propose an analytical framework for testing hypotheses regarding this behavior and its effects on the genetic structure of fish in an explicit geographical context, using a geographical genetics toolbox. Although disentangling the many potential causes underlying genetic population structure and unambiguously demonstrating that the homing behavior causes these genetic patterns is difficult, our framework allows the successive testing of homing behavior with increasing levels of complexity based on the following: (1) establishment of population structures among waterheads; (2) patterns of genetic variability throughout the adult migratory pool; (3) analyses of the non-migratory adult pool; and (4) comparisons among successive generations. We expect that the framework presented here will help delineating the appropriate uses of different sampling designs to make inferences regarding homing behavior and illustrate the limits imposed by the interpretation of different types of genetic data. More importantly, we hope this framework enables researchers to understand how a particular dataset can be utilized in a broader context as an ongoing part of a larger research program and thus guide future research by developing better and more integrated sampling designs.     

Understanding the genetic effects of recent habitat fragmentation in the context of evolutionary history: phylogeography and landscape genetics of a southern California endemic Jerusalem cricket (Orthoptera: Stenopelmatidae: Stenopelmatus)

Habitat loss and fragmentation due to urbanization are the most pervasive threats to biodiversity in southern California. Loss of habitat and fragmentation can lower migration rates and genetic connectivity among remaining populations of native species, reducing genetic variability and increasing extinction risk. However, it may be difficult to separate the effects of recent anthropogenic fragmentation from the genetic signature of prehistoric fragmentation due to previous natural geological and climatic changes. To address these challenges, we examined the phylogenetic and population genetic structure of a flightless insect endemic to cismontane southern California, Stenopelmatus'mahogani' (Orthoptera: Stenopelmatidae). Analyses of mitochondrial DNA sequence data suggest that diversification across southern California began during the Pleistocene, with most haplotypes currently restricted to a single population. Patterns of genetic divergence correlate with contemporary urbanization, even after correcting for (geographical information system) GIS-based reconstructions of fragmentation during the Pleistocene. Theoretical simulations confirm that contemporary patterns of genetic structure could be produced by recent urban fragmentation using biologically reasonable assumptions about model parameters. Diversity within populations was positively correlated with current fragment size, but not prehistoric fragment size, suggesting that the effects of increased drift following anthropogenic fragmentation are already being seen. Loss of genetic connectivity and diversity can hinder a population's ability to adapt to ecological perturbations commonly associated with urbanization, such as habitat degradation, climatic changes and introduced species. Consequently, our results underscore the importance of preserving and restoring landscape connectivity for long-term persistence of low vagility native species.     

Landscape features affect gene flow of Scottish Highland red deer (Cervus elaphus)

Landscape features have been shown to strongly influence dispersal and, consequently, the genetic population structure of organisms. Studies quantifying the effect of landscape features on gene flow of large mammals with high dispersal capabilities are rare and have mainly been focused at large geographical scales. In this study, we assessed the influence of several natural and human-made landscape features on red deer gene flow in the Scottish Highlands by analysing 695 individuals for 21 microsatellite markers. Despite the relatively small scale of the study area (115 × 87 km), significant population structure was found using F -statistics ( F _ST = 0.019) and the program structure , with major differentiation found between populations sampled on either side of the main geographical barrier (the Great Glen). To assess the effect of landscape features on red deer population structure, the ArcMap GIS was used to create cost-distance matrices for moving between populations, using a range of cost values for each of the landscape features under consideration. Landscape features were shown to significantly affect red deer gene flow as they explained a greater proportion of the genetic variation than the geographical distance between populations. Sea lochs were found to be the most important red deer gene flow barriers in our study area, followed by mountain slopes, roads and forests. Inland lochs and rivers were identified as landscape features that might facilitate gene flow of red deer. Additionally, we explored the effect of choosing arbitrary cell cost values to construct least cost-distance matrices and described a method for improving the selection of cell cost values for a particular landscape feature.     

Approximate Bayesian computation reveals the factors that influence genetic diversity and population structure of foxsnakes

Contemporary geographical range and patterns of genetic diversity within species reflect complex interactions between multiple factors acting across spatial and temporal scales, and it is notoriously difficult to disentangle causation. Here, we quantify patterns of genetic diversity and genetic population structure using mitochondrial DNA sequences (101 individuals, cytochrome b) and microsatellites (816 individuals, 12 loci) and use Approximate Bayesian computation methods to test competing models of the demographic history of eastern and western foxsnakes. Our analyses indicate that post-glacial colonization and past population declines, probably caused by the infilling of deciduous forest and cooler temperatures since the mid-Holocene, largely underpin large-scale genetic patterns for foxsnakes. At finer geographical scales, our results point to more recent anthropogenic habitat loss as having accentuated genetic population structure by causing further declines and fragmentation.     

Contrasting patterns of mitochondrial and microsatellite population structure in fragmented populations of greater prairie-chickens

Greater prairie-chickens (Tympanuchus cupido pinnatus) were once found throughout the tallgrass prairie of midwestern North America but over the last century these prairies have been lost or fragmented by human land use. As a consequence, many current populations of prairie-chickens have become isolated and small. This fragmentation of populations is expected to lead to reductions in genetic variation as a result of random genetic drift and a decrease in gene flow. As expected, we found that genetic variation at both microsatellite DNA and mitochondrial DNA (mtDNA) markers was reduced in smaller populations, particularly in Wisconsin. There was relatively little range-wide geographical structure (FST) when we examined mtDNA haplotypes but there was a significant positive relationship between genetic (FST) and geographical distance (isolation by distance). In contrast, microsatellite DNA loci revealed significant geographical structure (FST) and a weak effect of isolation by distance throughout the range. These patterns were much stronger when populations with reduced levels of genetic variability (Wisconsin) were removed from the analyses. This suggests that the effects of genetic drift were stronger than gene flow at microsatellite loci, whereas these forces were in range-wide equilibrium at mtDNA markers. These differences between the two molecular markers may be explained by a larger effective population size (Ne) for mtDNA, which is expected in species such as prairie-chickens that have female-biased dispersal and high levels of polygyny. Our results suggest that historic populations of prairie-chickens were once interconnected by gene flow but current populations are now isolated. Thus, maintaining gene flow may be important for the long-term persistence of prairie-chicken populations.     

Phylogeographical structure in the subterranean tuco-tuco Ctenomys talarum (Rodentia: Ctenomyidae): contrasting the demographic consequences of regional and habitat-specific histories

In this work we examined the phylogeography of the South American subterranean herbivorous rodent Ctenomys talarum (Talas tuco-tuco) using mitochondrial DNA (mtDNA) control region (D-loop) sequences, and we assessed the geographical genetic structure of this species in comparison with that of subterranean Ctenomys australis, which we have shown previously to be parapatric to C. talarum and to also live in a coastal sand dune habitat. A significant apportionment of the genetic variance among regional groups indicated that putative geographical barriers, such as rivers, substantially affected the pattern of genetic structure in C. talarum. Furthermore, genetic differentiation is consistent with a simple model of isolation by distance, possibly evidencing equilibrium between gene flow and local genetic drift. In contrast, C. australis showed limited hierarchical partitioning of genetic variation and departed from an isolation-by-distance pattern. Mismatch distributions and tests of neutrality suggest contrasting histories of these two species: C. talarum appears to be characterized by demographic stability and no significant departures from neutrality, whereas C. australis has undergone a recent demographic expansion and/or departures from strict neutrality in its mtDNA.     

An analysis of selection on a colour polymorphism in the northern leopard frog

In this study, we investigated the role of selection in the maintenance of a dorsal colour polymorphism in natural populations of the northern leopard frog, Rana pipiens. We determined genetic structure both spatially and temporally from a suite of putatively neutral molecular markers and tested whether or not the colour locus exhibited patterns of genetic variation that differed from those of the neutral loci. Spatial genetic structure at the colour locus was indistinguishable from structure at neutral loci [95% confidence intervals of F(ST) (neutral) = (0.07, 0.35), F(ST) (colour locus) = 0.114]. In the temporal analysis, we found that the variance among populations in the change in allele frequency at the colour locus (equal to 0.004) lies within the 95% confidence intervals for the variance among populations in changes in allele frequencies at neutral loci. In light of our inability to show evidence for the selective maintenance of the colour polymorphism, we used computer simulations to infer the power of our spatial and temporal techniques to detect selection. The computer simulations showed that although the strength of selection (s) would need to be relatively strong to have been detected by the temporal approach (s = 0.1-0.4, depending on the model tested), the spatial analysis would have detected all but weak selection (s = 0.01-0.04, depending on the model tested). This study illustrates the importance of using a locus comparison approach to detect evidence for selective maintenance before conducting studies to measure the selective mechanisms maintaining a polymorphism.     

Cryptic population structure in a large,mobile mammalian predator: the Scandinavian lynx

The Eurasian lynx (Lynx lynx) is an example of a species that has gone through a severe bottleneck, leading to near extinction in Scandinavia around 1930-- a pattern shared with several other large carnivorous mammals. Here we extend previous genetic analyses of northern European lynx, confirming that lynx from the Scandinavian Peninsula represent a distinct clade differing clearly from European conspecifics. Furthermore, and despite a recent bottleneck and subsequent range expansion, we detect marked genetic differentiation within Scandinavia. This differentiation is largely manifested as a north-south gradient, with a linear increase in the quantity FST/(1 - FST). Aided by computer simulations we find that this pattern is unlikely to have arisen by random genetic drift in the short time since lynx started to expand in the 1950s, suggesting that the spatial structure may predate the bottleneck. Individual-based analyses indicate that, instead of a continuous gradient, Scandinavian lynx may be structured into three more or less distinct groups, possibly corresponding to northern, central and southern subpopulations. The presence of such structuring was unknown previously and was unexpected from general considerations on the mobility of the species, historical data and the absence of geographical barriers. Our study demonstrates how molecular markers may be used to detect cryptic population structure, invisible using traditional methods.     

IIb‐RAD‐sequencing coupled with random forest classification indicates regional population structuring and sex‐specific differentiation in salmon lice (Lepeophtheirus salmonis)

The aquaculture industry has been dealing with salmon lice problems forming serious threats to salmonid farming. Several treatment approaches have been used to control the parasite. Treatment effectiveness must be optimized, and the systematic genetic differences between subpopulations must be studied to monitor louse species and enhance targeted control measures. We have used IIb‐RAD sequencing in tandem with a random forest classification algorithm to detect the regional genetic structure of the Norwegian salmon lice and identify important markers for sex differentiation of this species. We identified 19,428 single nucleotide polymorphisms (SNPs) from 95 individuals of salmon lice. These SNPs, however, were not able to distinguish the differential structure of lice populations. Using the random forest algorithm, we selected 91 SNPs important for geographical classification and 14 SNPs important for sex classification. The geographically important SNP data substantially improved the genetic understanding of the population structure and classified regional demographic clusters along the Norwegian coast. We also uncovered SNP markers that could help determine the sex of the salmon louse. A large portion of the SNPs identified to be under directional selection was also ranked highly important by random forest. According to our findings, there is a regional population structure of salmon lice associated with the geographical location along the Norwegian coastline.     

Two-generation analysis of pollen flow across a landscape V: a stepwise approach for extracting factors contributing to pollen structure

Patterns of pollen dispersal are central to both the ecology and evolution of plant populations. However, the mechanisms controlling either the dispersal process itself or our estimation of that process may be influenced by site-specific factors such as local forest structure and nonuniform adult genetic structure. Here, we present an extension of the AMOVA model applied to the recently developed TWOGENER analysis of pollen pool structure. This model, dubbed the Stepwise AMOVA (StAMOVA), focuses on determining to what extent ecological, demographic, and/or environmental factors influence the observed genetic variation in spatially separated pollen pools. The analysis is verified for efficacy, using an extensive battery of simulations, illustrating: (1) how nonuniform adult genetic structure influences the differentiation of spatially separated pollen pools, and (2) how effectively the Stepwise analysis performs in carrying out the appropriate corrections. Finally, the model is applied to a Quercus alba data set, from which we have prior evidence that the adult genetic structure is nonuniformly distributed across the sampling landscape. From this data set, we show how the Stepwise model can be applied to remove the effects of spatial adult genetic structure on pollen pool differentiation and contrast these results with those derived from the original TWOGENER analysis.