Social and spatial effects on genetic variation between foraging flocks in a wild bird population

Social interactions are rarely random. In some instances, animals exhibit homophily or heterophily, the tendency to interact with similar or dissimilar conspecifics, respectively. Genetic homophily and heterophily influence the evolutionary dynamics of populations, because they potentially affect sexual and social selection. Here, we investigate the link between social interactions and allele frequencies in foraging flocks of great tits (Parus major) over three consecutive years. We constructed co‐occurrence networks which explicitly described the splitting and merging of 85,602 flocks through time (fission–fusion dynamics), at 60 feeding sites. Of the 1,711 birds in those flocks, we genotyped 962 individuals at 4,701 autosomal single nucleotide polymorphisms (SNPs). By combining genomewide genotyping with repeated field observations of the same individuals, we were able to investigate links between social structure and allele frequencies at a much finer scale than was previously possible. We explicitly accounted for potential spatial effects underlying genetic structure at the population level. We modelled social structure and spatial configuration of great tit fission–fusion dynamics with eigenvector maps. Variance partitioning revealed that allele frequencies were strongly affected by group fidelity (explaining 27%–45% of variance) as individuals tended to maintain associations with the same conspecifics. These conspecifics were genetically more dissimilar than expected, shown by genomewide heterophily for pure social (i.e., space‐independent) grouping preferences. Genomewide homophily was linked to spatial configuration, indicating spatial segregation of genotypes. We did not find evidence for homophily or heterophily for putative socially relevant candidate genes or any other SNP markers. Together, these results demonstrate the importance of distinguishing social and spatial processes in determining population structure.     

Population structure over a broad spatial scale driven by nonanthropogenic factors in a wide‐ranging migratory mammal,Alaskan caribou

Wide‐ranging mammals face significant conservation threats, and knowledge of the spatial scale of population structure and its drivers is needed to understand processes that maintain diversity in these species. We analysed DNA from 655 Alaskan caribou (Rangifer tarandus granti) from 20 herds that vary in population size, used 19 microsatellite loci to document genetic diversity and differentiation in Alaskan caribou, and examined the extent to which genetic differentiation was associated with hypothesized drivers of population subdivision including landscape features, population size and ecotype. We found that Alaskan caribou are subdivided into two hierarchically structured clusters: one group on the Alaska Peninsula containing discrete herds and one large group on the Mainland lacking differentiation between many herds. Population size, geographic distance, migratory ecotype and the Kvichak River at the nexus of the Alaska Peninsula were associated with genetic differentiation. Contrary to previous hypotheses, small Mainland herds were often differentiated genetically from large interconnected herds nearby, and genetic drift coupled with reduced gene flow may explain this pattern. Our results raise the possibility that behaviour helps to maintain genetic differentiation between some herds of different ecotypes. Alaskan caribou show remarkably high diversity and low differentiation over a broad geographic scale. These results increase information for the conservation of caribou and other migratory mammals threatened by population reductions and landscape barriers and may be broadly applicable to understanding the spatial scale and ecological drivers of population structure in widespread species.     

Population structure of caribou in an ice‐bound archipelago

Aim

Archipelagos provide ideal natural systems for testing the effects of isolation and fragmentation of habitats on the genetic makeup of populations—an important consideration, given that many insular species are of conservation concern. Two theories predominate: Island Biogeography Theory (IBT) posits that proximity to the mainland drives the potential for migrants and gene flow. The Central Marginal Hypothesis (CMH) predicts that island populations at the periphery of a species range may experience low gene flow, small population size and high rates of genetic drift. We investigated population genetic structure, genetic diversity and key drivers of diversity for Arctic island‐dwelling caribou (Rangifer tarandus). Our aim was to inform intraspecific units for conservation and decipher how IBT and CMH could act in an archipelago where isolation is highly variable due to sea ice and open water.

Location

Canadian Arctic Archipelago, Canada (Latitude, 55–82°N; Longitude, 61–123°W).

Methods

We genotyped 447 caribou at 16 microsatellite loci; these caribou represented two subspecies (R. t. groenlandicus, R. t. pearyi) and three designatable units. We used hierarchical Bayesian clustering and ordination to determine genetic groups. We evaluated the influence of ecological and geographic variables on genetic diversity using linear mixed‐effects models and compared diversity among mainland and island herds.

Results

Bayesian clustering revealed nine genetic clusters with differentiation among and within caribou subspecies. Genetic differentiation was explained predominantly by isolation‐by‐distance across all caribou, even at the scale of subspecies. Island caribou were less genetically diverse than mainland herds; individual heterozygosity was negatively correlated with distance‐to‐mainland and the extent of autumn ice‐free coastline and positively correlated with unglaciated island size.

Main conclusions

Our findings underscore the importance of hierarchical analysis when investigating genetic population structure. Genetic diversity and its key drivers lend support to both IBT and CMH and highlight the pending threat of climate change for Arctic island caribou.

     

Seascape drivers of Macrocystis pyrifera population genetic structure in the northeast Pacific

At small spatial and temporal scales, genetic differentiation is largely controlled by constraints on gene flow, while genetic diversity across a species' distribution is shaped on longer temporal and spatial scales. We assess the hypothesis that oceanographic transport and other seascape features explain different scales of genetic structure of giant kelp, Macrocystis pyrifera. We followed a hierarchical approach to perform a microsatellite‐based analysis of genetic differentiation in Macrocystis across its distribution in the northeast Pacific. We used seascape genetic approaches to identify large‐scale biogeographic population clusters and investigate whether they could be explained by oceanographic transport and other environmental drivers. We then modelled population genetic differentiation within clusters as a function of oceanographic transport and other environmental factors. Five geographic clusters were identified: Alaska/Canada, central California, continental Santa Barbara, California Channel Islands and mainland southern California/Baja California peninsula. The strongest break occurred between central and southern California, with mainland Santa Barbara sites forming a transition zone between the two. Breaks between clusters corresponded approximately to previously identified biogeographic breaks, but were not solely explained by oceanographic transport. An isolation‐by‐environment (IBE) pattern was observed where the northern and southern Channel Islands clustered together, but not with closer mainland sites, despite the greater distance between them. The strongest environmental association with this IBE pattern was observed with light extinction coefficient, which extends suitable habitat to deeper areas. Within clusters, we found support for previous results showing that oceanographic connectivity plays an important role in the population genetic structure of Macrocystis in the Northern hemisphere.     

Assessing the geographic scale of genetic population management with microsatellites and introns in the clam Ruditapes decussatus

The clam Ruditapes decussatus is commercially important in southwestern Europe, suffering from population decline and hybridization with exotic Manila clam (R. philippinarum). Previous studies with intronic markers showed a genetic subdivision of the species in three races (Atlantic, West Mediterranean, and Adriatic‐Aegean). However, detailed population genetic studies to help management of the main production areas in the southwest of Europe are missing. We have analyzed eight Atlantic and two Mediterranean populations from the Spanish coasts using 14 microsatellites and six intronic markers. Microsatellites confirmed the Atlantic and West Mediterranean races detected with introns and showed that genetic variability was higher in Mediterranean than in Atlantic populations. Both marker types showed that genetic differentiation of Atlantic populations was low and indicated that populations could be managed at the regional level in the case of Cantabrian and Gulf of Cadiz areas, but not in the case of Rias Baixas and the Mediterranean. This study shows the interest of including different types of markers in studies of genetic population structure of marine organisms.     

Environmental variation shapes genetic variation in Bouteloua gracilis: Implications for restoration management of natural populations and cultivated varieties in the southwestern United States

With the increasing frequency of large‐scale restoration efforts, the need to understand the adaptive genetic structure of natural plant populations and their relation to heavily utilized cultivars is critical. Bouteloua gracilis (blue grama) is a wind‐dispersed, perennial grass consisting of several cytotypes (2n = 2×–6×) with a widespread distribution in western North America. The species is locally dominant and used regularly in restoration treatments. Using amplified fragment length polymorphism (AFLP) and cpDNA analyses, we assessed the genetic variability and adaptive genetic structure of blue grama within and among 44 sampling sites that are representative of the species’ environmental and habitat diversity in the southwestern United States. Five cultivars were also included to investigate genetic diversity and differentiation in natural versus cultivated populations. Three main findings resulted from this study: (a) Ninety‐four polymorphic AFLP markers distinguished two population clusters defined largely by samples on and off the Colorado Plateau; (b) substructure of samples on the Colorado Plateau was indicated by genetic divergence between boundary and interior regions, and was supported by cytotype distribution and cpDNA analysis; and (c) six AFLP markers were identified as “outliers,” consistent with being under selection. These loci were significantly correlated to mean annual temperature, mean annual precipitation, precipitation of driest quarter, and precipitation of wettest quarter in natural populations, but not in cultivated samples. Marker × environment relationships were found to be largely influenced by cytotype and cultivar development. Our results demonstrate that blue grama is genetically variable, and exhibits genetic structure, which is shaped, in part, by environmental variability across the Colorado Plateau. Information from our study can be used to guide the selection of seed source populations for commercial development and long‐term conservation management of B. gracilis, which could include genetic assessments of diversity and the adaptive potential of both natural and cultivated populations for wildland restoration.     

Landscape variability explains spatial pattern of population structure of northern pike (Esox lucius) in a large fluvial system

A growing number of studies have been investigating the influence of contemporary environmental factors on population genetic structure, but few have addressed the issue of spatial patterns in the variable intensity of factors influencing the extent of population structure, and particularly so in aquatic ecosystems. In this study, we document the landscape genetics of northern pike (Esox lucius), based on the analysis of nearly 3000 individuals from 40 sampling sites using 22 microsatellites along the Lake Ontario – St. Lawrence River system (750 km) that locally presents diverse degrees of interannual water level variation. Genetic structure was globally very weak (F_ST = 0.0208) but spatially variable with mean level of differentiation in the upstream section of the studied area being threefold higher (F_ST = 0.0297) than observed in the downstream sector (F_ST = 0.0100). Beside interannual water level fluctuation, 19 additional variables were considered and a multiple regression on distance matrices model (R² = 0.6397, P < 0.001) revealed that water masses (b = 0.3617, P < 0.001) and man‐made dams (b = 0.4852, P < 0.005) reduced genetic connectivity. Local level of interannual water level stability was positively associated to the extent of genetic differentiation (b = 0.3499, P < 0.05). As water level variation impacts on yearly quality and localization of spawning habitats, our study illustrates how temporal variation in local habitat availability, caused by interannual water level fluctuations, may locally decrease population genetic structure by forcing fish to move over longer distances to find suitable habitat. This study thus represents one of the rare examples of how environmental fluctuations may influence spatial variation in the extent of population genetic structure within a given species.     

Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program structure

Reproducibility is the benchmark for results and conclusions drawn from scientific studies, but systematic studies on the reproducibility of scientific results are surprisingly rare. Moreover, many modern statistical methods make use of ‘random walk’ model fitting procedures, and these are inherently stochastic in their output. Does the combination of these statistical procedures and current standards of data archiving and method reporting permit the reproduction of the authors' results? To test this, we reanalysed data sets gathered from papers using the software package structure to identify genetically similar clusters of individuals. We find that reproducing structure results can be difficult despite the straightforward requirements of the program. Our results indicate that 30% of analyses were unable to reproduce the same number of population clusters. To improve this, we make recommendations for future use of the software and for reporting structure analyses and results in published works.     

Landscape genetics of a specialized grasshopper inhabiting highly fragmented habitats: a role for spatial scale

Aim The study of geographical discontinuities in the distribution of genetic variability in natural populations is a central topic in both evolutionary and conservation research. In this study, we aimed to analyse (1) the factors associated with genetic diversity at the landscape spatial scale in the highly specialized grasshopper Mioscirtus wagneri and (2) to identify the relative contribution of alternative factors to the observed patterns of genetic structure in this species. Location La Mancha region, Central Spain. Methods We sampled 28 populations of the grasshopper M. wagneri and genotyped 648 individuals at seven microsatellite loci. We employed a causal modelling approach to identify the most influential variables associated with genetic differentiation within a multiple hypothesis‐testing framework. Results We found that genetic diversity differs among populations located in different river basins and decreases with population isolation. Causal modelling analyses showed variability in the relative influence of the studied landscape features across different spatial scales. When a highly isolated population is considered, the analyses suggested that geographical distance is the only factor explaining the genetic differentiation between populations. When that population is excluded, the causal modelling analysis revealed that elevation and river basins are also relevant factors contributing to explaining genetic differentiation between the studied populations. Main conclusions These results indicate that the spatial scale considered and the inclusion of outlier populations may have important consequences on the inferred contribution of alternative landscape factors on the patterns of genetic differentiation even when all populations are expected to similarly respond to landscape structure. Thus, a multiscale perspective should also be incorporated into the landscape genetics framework to avoid biased conclusions derived from the spatial scale analysed and/or the geographical distribution of the studied populations.     

Landscape characteristics influencing the genetic structure of greater sage‐grouse within the stronghold of their range: a holistic modeling approach

Given the significance of animal dispersal to population dynamics and geographic variability, understanding how dispersal is impacted by landscape patterns has major ecological and conservation importance. Speaking to the importance of dispersal, the use of linear mixed models to compare genetic differentiation with pairwise resistance derived from landscape resistance surfaces has presented new opportunities to disentangle the menagerie of factors behind effective dispersal across a given landscape. Here, we combine these approaches with novel resistance surface parameterization to determine how the distribution of high‐ and low‐quality seasonal habitat and individual landscape components shape patterns of gene flow for the greater sage‐grouse (Centrocercus urophasianus) across Wyoming. We found that pairwise resistance derived from the distribution of low‐quality nesting and winter, but not summer, seasonal habitat had the strongest correlation with genetic differentiation. Although the patterns were not as strong as with habitat distribution, multivariate models with sagebrush cover and landscape ruggedness or forest cover and ruggedness similarly had a much stronger fit with genetic differentiation than an undifferentiated landscape. In most cases, landscape resistance surfaces transformed with 17.33‐km‐diameter moving windows were preferred, suggesting small‐scale differences in habitat were unimportant at this large spatial extent. Despite the emergence of these overall patterns, there were differences in the selection of top models depending on the model selection criteria, suggesting research into the most appropriate criteria for landscape genetics is required. Overall, our results highlight the importance of differences in seasonal habitat preferences to patterns of gene flow and suggest the combination of habitat suitability modeling and linear mixed models with our resistance parameterization is a powerful approach to discerning the effects of landscape on gene flow.     

Noninvasive sampling reveals population genetic structure in the Royle’s pika,Ochotona roylei,in the western Himalaya

Understanding population genetic structure of climate‐sensitive herbivore species is important as it provides useful insights on how shifts in environmental conditions can alter their distribution and abundance. Herbivore responses to the environment can have a strong indirect cascading effect on community structure. This is particularly important for Royle's pika (Lagomorpha: Ochotona roylei), a herbivorous talus‐dwelling species in alpine ecosystem, which forms a major prey base for many carnivores in the Himalayan arc. In this study, we used seven polymorphic microsatellite loci to detect evidence for recent changes in genetic diversity and population structure in Royle's pika across five locations sampled between 8 and 160 km apart in the western Himalaya. Using four clustering approaches, we found the presence of significant contemporary genetic structure in Royle's pika populations. The detected genetic structure could be primarily attributed to the landscape features in alpine habitat (e.g., wide lowland valleys, rivers) that may act as semipermeable barriers to gene flow and distribution of food plants, which are key determinants in spatial distribution of herbivores. Pika showed low inbreeding coefficients (F_IS) and a high level of pairwise relatedness for individuals within 1 km suggesting low dispersal abilities of talus‐dwelling pikas. We have found evidence of a recent population bottleneck, possibly due to effects of environmental disturbances (e.g., snow melting patterns or thermal stress). Our results reveal significant evidence of isolation by distance in genetic differentiation (F_ST range = 0.04–0.19). This is the first population genetics study on Royle's pika, which helps to address evolutionary consequences of climate change which are expected to significantly affect the distribution and population dynamics in this talus‐dwelling species.     

mmod: an R library for the calculation of population differentiation statistics

mmod is a library for the R programming language that allows the calculation of the population differentiation measures D_est, G″_ST and φ′_ST. R provides a powerful environment in which to conduct and record population genetic analyses but, at present, no R libraries provide functions for the calculation of these statistics from standard population genetic files. In addition to the calculation of differentiation measures, mmod can produce parametric bootstrap and jackknife samples of data sets for further analysis. By integrating with and complimenting the existing libraries adegenet and pegas , mmod extends the power of R as a population genetic platform.     

Assessment of spatial genetic structure to identify populations at risk for infection of an emerging epizootic disease

1. Understanding the geographic extent and connectivity of wildlife populations can provide important insights into the management of disease outbreaks but defining patterns of population structure is difficult for widely distributed species. Landscape genetic analyses are powerful methods for identifying cryptic structure and movement patterns that may be associated with spatial epizootic patterns in such cases.
2. We characterized patterns of population substructure and connectivity using microsatellite genotypes from 2,222 white‐tailed deer (Odocoileus virginianus) in the Mid‐Atlantic region of the United States, a region where chronic wasting disease was first detected in 2009. The goal of this study was to evaluate the juxtaposition between population structure, landscape features that influence gene flow, and current disease management units.
3. Clustering analyses identified four to five subpopulations in this region, the edges of which corresponded to ecophysiographic provinces. Subpopulations were further partitioned into 11 clusters with subtle (F_ST ≤ 0.041), but significant genetic differentiation. Genetic differentiation was lower and migration rates were higher among neighboring genetic clusters, indicating an underlying genetic cline. Genetic discontinuities were associated with topographic barriers, however.
4. Resistance surface modeling indicated that gene flow was diffuse in homogenous landscapes, but the direction and extent of gene flow were influenced by forest cover, traffic volume, and elevational relief in subregions heterogeneous for these landscape features. Chronic wasting disease primarily occurred among genetic clusters within a single subpopulation and along corridors of high landscape connectivity.
5. These results may suggest a possible correlation between population substructure, landscape connectivity, and the occurrence of diseases for widespread species. Considering these factors may be useful in delineating effective management units, although only the largest features produced appreciable differences in subpopulation structure. Disease mitigation strategies implemented at the scale of ecophysiographic provinces are likely to be more effective than those implemented at finer scales.

     

景观遗传学原理及其在生境片断化遗传效应研究中的应用

景观遗传学是近年来在景观生态学和种群遗传学之间形成的一个交叉领域,强调景观的组成、空间构型和环境梯度对基因流、种群遗传空间结构和局域种群适应的影响。景观遗传学尚未成为一门独立的学科,其理论基础主要来自分子遗传学、种群生物学和景观生态学。现代分子遗传标记技术、遥感和GIS支持下的景观分析和空间统计方法的综合运用是景观遗传学主要研究途径。系统介绍了景观遗传学的基础概念,关键科学问题,基本理论框架,及其与相邻研究领域的关系,综述了景观遗传学最为关注的现实课题——景观碎裂化的种群遗传效应的研究进展,主要涉及生境片断化的遗传效应、不同属性的物种响应、以及生境片断化过程的选择作用等方面。通过采取一种跨尺度的视角,景观遗传学研究显著深化了关于景观碎裂化对生物多样性影响的理解。     

Optimizing the trade‐off between spatial and genetic sampling efforts in patchy populations: towards a better assessment of functional connectivity using an individual‐based sampling scheme

Genetic data are increasingly used in landscape ecology for the indirect assessment of functional connectivity, that is, the permeability of landscape to movements of organisms. Among available tools, matrix correlation analyses (e.g. Mantel tests or mixed models) are commonly used to test for the relationship between pairwise genetic distances and movement costs incurred by dispersing individuals. When organisms are spatially clustered, a population‐based sampling scheme (PSS) is usually performed, so that a large number of genotypes can be used to compute pairwise genetic distances on the basis of allelic frequencies. Because of financial constraints, this kind of sampling scheme implies a drastic reduction in the number of sampled aggregates, thereby reducing sampling coverage at the landscape level. We used matrix correlation analyses on simulated and empirical genetic data sets to investigate the efficiency of an individual‐based sampling scheme (ISS) in detecting isolation‐by‐distance and isolation‐by‐barrier patterns. Provided that pseudo‐replication issues are taken into account (e.g. through restricted permutations in Mantel tests), we showed that the use of interindividual measures of genotypic dissimilarity may efficiently replace interpopulation measures of genetic differentiation: the sampling of only three or four individuals per aggregate may be sufficient to efficiently detect specific genetic patterns in most situations. The ISS proved to be a promising methodological alternative to the more conventional PSS, offering much flexibility in the spatial design of sampling schemes and ensuring an optimal representativeness of landscape heterogeneity in data, with few aggregates left unsampled. Each strategy offering specific advantages, a combined use of both sampling schemes is discussed.     

Consequences of multiple mating‐system shifts for population and range‐wide genetic structure in a coastal dune plant

Evolutionary transitions from outcrossing to selfing can strongly affect the genetic diversity and structure of species at multiple spatial scales. We investigated the genetic consequences of mating‐system shifts in the North American, Pacific coast dune endemic plant Camissoniopsis cheiranthifolia (Onagraceae) by assaying variation at 13 nuclear (n) and six chloroplast (cp) microsatellite (SSR) loci for 38 populations across the species range. As predicted from the expected reduction in effective population size (N_e) caused by selfing, small‐flowered, predominantly selfing (SF) populations had much lower nSSR diversity (but not cpSSR) than large‐flowered, predominantly outcrossing (LF) populations. The reduction in nSSR diversity was greater than expected from the effects of selfing on N_e alone, but could not be accounted for by indirect effects of selfing on population density. Although selfing should reduce gene flow, SF populations were not more genetically differentiated than LF populations. We detected five clusters of nSSR genotypes and three groups of cpSSR haplotypes across the species range consisting of parapatric groups of populations that usually (but not always) differed in mating system, suggesting that selfing may often initiate ecogeographic isolation. However, lineage‐wide genetic variation was not lower for selfing clusters, failing to support the hypothesis that selection for reproductive assurance spurred the evolution of selfing in this species. Within three populations where LF and SF plants coexist, we detected genetic differentiation among diverged floral phenotypes suggesting that reproductive isolation (probably postzygotic) may help maintain the striking mating‐system differentiation observed across the range of this species.     

Rise and fall of a wolf population: genetic diversity and structure during recovery,rapid expansion and drastic decline

The grey wolves (Canis lupus) of Finland have had a varied history, with a period of rapid population expansion after the mid‐1990s followed by a decline with a current census size of about 140 wolves. Here, we investigate the impact of unstable population size and connectivity on genetic diversity and structure in a long‐term genetic study of 298 Finnish wolves born in 1995–2009 and genotyped for 17 microsatellite loci. During the initial recovery and prior to population expansion, genetic diversity was high (1995–1997: LD‐N_e = 67.2; H_o = 0.749; H_e = 0.709) despite a small census size and low number of breeders (N_c < 100; N_b < 10) likely reflecting the status of the Russian source population. Surprisingly, observed heterozygosity decreased significantly during the study period (t = ?2.643, P = 0.021) despite population expansion, likely a result of an increase in inbreeding (F_IS = 0.108 in 2007–2009) owing to a low degree of connectivity with adjacent Russian wolf population (m = 0.016–0.090; F_ST = 0.086, P < 0.001) and population crash after 2006. However, population growth had a temporary positive impact on N_e and number of family lines. This study shows that even strong population growth alone might not be adequate to retain genetic diversity, especially when accompanied with low amount of subsequent gene flow and population decline.     

Genetic diagnosis of a rare myrmecochorous species,Plagiorhegma dubium (Berberidaceae): Historical genetic bottlenecks and strong spatial structures among populations

Distribution of genetic variation over time and space is relevant to demographic histories and tightly linked to ecological disturbances as well as evolutionary potential of an organism. Therefore, understanding the pattern of genetic diversity is a primary step in conservation and management projects for rare and threatened plant species. We used eight microsatellite markers to examine the level of genetic diversity, spatial structure, and demographic history of Plagiorhegma dubium, a rare myrmecochorous herb, populations sampled across northeast Asia and Siberia. We found low within‐population genetic variation associated with historical bottlenecks. Although pairwise F_ST values were not much higher than the ones found in similar life form species, STRUCTURE and PCoA revealed a clear broadscale spatial pattern of genetic structure. Bayesian clustering (best K = 6) and PCoA identified three populations that are distinctive from neighboring populations in the Korean peninsula, which suggests potential units for conservation and management plans in Korea. MIGRATE‐N and BAYESASS showed that both contemporary (0.003–0.045) and historical migration rates (2 × e^?5?4.6 × e^?4) were low. Our findings provide a good example, where genetic considerations should be integrated for conservation and management plans of rare and threatened species.