Population genomics of the killer whale indicates ecotype evolution in sympatry involving both selection and drift

The evolution of diversity in the marine ecosystem is poorly understood, given the relatively high potential for connectivity, especially for highly mobile species such as whales and dolphins. The killer whale (Orcinus orca) has a worldwide distribution, and individual social groups travel over a wide geographic range. Even so, regional populations have been shown to be genetically differentiated, including among different foraging specialists (ecotypes) in sympatry. Given the strong matrifocal social structure of this species together with strong resource specializations, understanding the process of differentiation will require an understanding of the relative importance of both genetic drift and local adaptation. Here we provide a high‐resolution analysis based on nuclear single‐nucleotide polymorphic markers and inference about differentiation at both neutral loci and those potentially under selection. We find that all population comparisons, within or among foraging ecotypes, show significant differentiation, including populations in parapatry and sympatry. Loci putatively under selection show a different pattern of structure compared to neutral loci and are associated with gene ontology terms reflecting physiologically relevant functions (e.g. related to digestion). The pattern of differentiation for one ecotype in the North Pacific suggests local adaptation and shows some fixed differences among sympatric ecotypes. We suggest that differential habitat use and resource specializations have promoted sufficient isolation to allow differential evolution at neutral and functional loci, but that the process is recent and dependent on both selection and drift.     

Social cohesion among kin,gene flow without dispersal and the evolution of population genetic structure in the killer whale (Orcinus orca)

In social species, breeding system and gregarious behavior are key factors influencing the evolution of large‐scale population genetic structure. The killer whale is a highly social apex predator showing genetic differentiation in sympatry between populations of foraging specialists (ecotypes), and low levels of genetic diversity overall. Our comparative assessments of kinship, parentage and dispersal reveal high levels of kinship within local populations and ongoing male‐mediated gene flow among them, including among ecotypes that are maximally divergent within the mtDNA phylogeny. Dispersal from natal populations was rare, implying that gene flow occurs without dispersal, as a result of reproduction during temporary interactions. Discordance between nuclear and mitochondrial phylogenies was consistent with earlier studies suggesting a stochastic basis for the magnitude of mtDNA differentiation between matrilines. Taken together our results show how the killer whale breeding system, coupled with social, dispersal and foraging behaviour, contributes to the evolution of population genetic structure.     

Phylogenomics of the killer whale indicates ecotype divergence in sympatry

For many highly mobile species, the marine environment presents few obvious barriers to gene flow. Even so, there is considerable diversity within and among species, referred to by some as the ‘marine speciation paradox''. The recent and diverse radiation of delphinid cetaceans (dolphins) represents a good example of this. Delphinids are capable of extensive dispersion and yet many show fine-scale genetic differentiation among populations. Proposed mechanisms include the division and isolation of populations based on habitat dependence and resource specializations, and habitat release or changing dispersal corridors during glacial cycles. Here we use a phylogenomic approach to investigate the origin of differentiated sympatric populations of killer whales (Orcinus orca). Killer whales show strong specialization on prey choice in populations of stable matrifocal social groups (ecotypes), associated with genetic and phenotypic differentiation. Our data suggest evolution in sympatry among populations of resource specialists.     

Ecotypes of an ecologically dominant prairie grass (Andropogon gerardii) exhibit genetic divergence across the U.S. Midwest grasslands' environmental gradient

Big bluestem (Andropogon gerardii) is an ecologically dominant grass with wide distribution across the environmental gradient of U.S. Midwest grasslands. This system offers an ideal natural laboratory to study population divergence and adaptation in spatially varying climates. Objectives were to: (i) characterize neutral genetic diversity and structure within and among three regional ecotypes derived from 11 prairies across the U.S. Midwest environmental gradient, (ii) distinguish between the relative roles of isolation by distance (IBD) vs. isolation by environment (IBE) on ecotype divergence, (iii) identify outlier loci under selection and (iv) assess the association between outlier loci and climate. Using two primer sets, we genotyped 378 plants at 384 polymorphic AFLP loci across regional ecotypes from central and eastern Kansas and Illinois. Neighbour‐joining tree and PCoA revealed strong genetic differentiation between Kansas and Illinois ecotypes, which was better explained by IBE than IBD. We found high genetic variability within prairies (80%) and even fragmented Illinois prairies, surprisingly, contained high within‐prairie genetic diversity (92%). Using Bayenv 2, 14 top‐ranked outlier loci among ecotypes were associated with temperature and precipitation variables. Six of seven BayeScan F_ST outliers were in common with Bayenv 2 outliers. High genetic diversity may enable big bluestem populations to better withstand changing climates; however, population divergence supports the use of local ecotypes in grassland restoration. Knowledge of genetic variation in this ecological dominant and other grassland species will be critical to understanding grassland response and restoration challenges in the face of a changing climate.     

Using a multi-disciplinary approach to identify a critically endangered killer whale management unit

A key goal for wildlife managers is identifying discrete, demographically independent conservation units. Previous genetic work assigned killer whales that occur seasonally in the Strait of Gibraltar (SoG) and killer whales sampled off the Canary Islands (CI) to the same population. Here we present new analyses of photo-identification and individual genotypes to assess the level of contemporary gene flow and migration between study areas, and analyses of biomarkers to assess ecological differences. We identified 47 different individuals from 5 pods in the SoG and 16 individuals in the CI, with no matches found between the areas. Mitochondrial DNA control region haplotype was shared by all individuals sampled within each pod, suggesting that pods have a matrifocal social structure typical of this species, whilst the lack of shared mitogenome haplotypes between the CI and SoG individuals suggests that there was little or no female migration between groups. Kinship analysis detected no close kin between CI and SoG individuals, and low to zero contemporary gene flow. Isotopic values and organochlorine pollutant loads also suggest ecological differences between study areas. We further found that one individual from a pod within the SoG not seen in association with the other four pods and identified as belonging to a potential migrant lineage by genetic analyses, had intermediate isotopic values and contaminant between the two study areas. Overall our results suggest a complex pattern of social and genetic structuring correlated with ecological variation. Consequently at least CI and SoG should be considered as two different management units. Understanding this complexity appears to be an important consideration when monitoring and understanding the viability of these management units. Understand the viability will help the conservation of these threatened management units.     

Low worldwide genetic diversity in the killer whale (Orcinus orca): implications for demographic history

A low level of genetic variation in mammalian populations where the census population size is relatively large has been attributed to various factors, such as a naturally small effective population size, historical bottlenecks and social behaviour. The killer whale (Orcinus orca) is an abundant, highly social species with reduced genetic variation. We find no consistent geographical pattern of global diversity and no mtDNA variation within some regional populations. The regional lack of variation is likely to be due to the strict matrilineal expansion of local populations. The worldwide pattern and paucity of diversity may indicate a historical bottleneck as an additional factor.     

Site-specific genetic divergence in parallel hybrid zones suggests nonallopatric evolution of reproductive barriers

The evolution of reproductive isolation in the presence of gene flow is supported by theoretical models but rarely by data. Empirical support might be gained from studies of parallel hybrid zones between interbreeding taxa. We analysed gene flow over two hybrid zones separating ecotypes of Littorina saxatilis to test the expectation that neutral genetic markers will show site-specific differences if barriers have evolved in situ. Distinct ecotypes found in contrasting shore habitats are separated by divergent selection and poor dispersal, but hybrid zones appear between them. Swedish islands formed by postglacial uplift 5000 years ago provide opportunities to assess genetic structure in a recently evolved system. Each island houses a discrete population containing subpopulations of different ecotypes. Hybrid zones between ecotypes may be a product of ecological divergence occurring on each island or a consequence of secondary overlap of ecotypes of allopatric origin that have spread among the islands. We used six microsatellite loci to assess gene flow and genetic profiles of hybrid zones on two islands. We found reduced gene flow over both hybrid zones, indicating the presence of local reproductive barriers between ecotypes. Nevertheless, subpopulations of different ecotypes from the same island were genetically more similar to each other than were subpopulations of the same ecotype from different islands. Moreover, neutral genetic traits separating the two ecotypes across hybrid zones were site-specific. This supports a scenario of in situ origin of ecotypes by ecological divergence and nonallopatric evolution of reproductive barriers.     

Linking genetic and ecological differentiation in an ungulate with a circumpolar distribution

Genetic differentiation among populations may arise from the disruption of gene flow due to local adaptation to distinct environments and/or neutral accumulation of mutations and genetic drift resulted from geographical isolation. Quantifying the role of these processes in determining the genetic structure of natural populations remains challenging. Here, we analyze the relative contribution of isolation‐by‐resistance (IBR), isolation‐by‐environment (IBE), genetic drift and historical isolation in allopatry during Pleistocene glacial cycles on shaping patterns of genetic differentiation in caribou/reindeer populations Rangifer tarandus across the entire distribution range of the species. Our study integrates analyses at range‐wide and regional scales to partial out the effects of historical and contemporary isolation mechanisms. At the circumpolar scale, our results indicate that genetic differentiation is predominantly explained by IBR and historical isolation. At a regional scale, we found that IBR, IBE and population size significantly explained the spatial distribution of genetic variation among populations belonging to the Euro‐Beringian lineage within North America. In contrast, genetic differentiation among populations within the North American lineage was predominantly explained by IBR and population size, but not IBE. We also found discrepancies between genetic and ecotype designation across the Holarctic species distribution range. Overall, these results indicate that multiple isolating mechanisms have played roles in shaping the spatial distribution of genetic variation across the distribution range of a large mammal with high potential for gene flow. Considering multiple spatial scales and simultaneously testing a comprehensive suite of potential isolating mechanisms, our study contributes to understand the ecological and evolutionary processes underlying organism–landscape interactions.     

Genetic differentiation and estimation of effective population size and migration rates in two sympatric ecotypes of the marine snail Littorina saxatilis

On exposed rocky shores in Galicia (northwest Spain), a striking polymorphism exists between two ecotypes (RB and SU) of Littorina saxatilis that occupy different levels of the intertidal zone and exhibit an incomplete reproductive isolation. The setting has been suggested to represent ongoing sympatric speciation by ecological adaptation of the two ecotypes to their respective habitats. In this article we address whether or not the ecotypes have developed their own population structures in response to the rigors of their corresponding environments and life histories. We analyzed four to five allozymic loci from three surveys of the same sites, spanning a 14-year period. An experimental design including three localities with two transects per locality and three shore levels allowed studying temporal and spatial population structure and estimation of effective population sizes (N(e)), neighborhood sizes (N(n)), and migration rates (m). Genetic differentiation was significantly lower in RB populations (theta(ST) = 0.067) than in SU ones (theta(ST) = 0.124). Mean estimates of N(e), N(n), and m did not differ significantly between ecotypes, but local ecotype differences in migration between the two closest localities (larger migration rates in RB than in SU populations) could explain the pattern in population differentiation.     

Highly Replicated Evolution of Parapatric Ecotypes

Parallel evolution of ecotypes occurs when selection independently drives the evolution of similar traits across similar environments. The multiple origins of ecotypes are often inferred based on a phylogeny that clusters populations according to geographic location and not by the environment they occupy. However, the use of phylogenies to infer parallel evolution in closely related populations is problematic because gene flow and incomplete lineage sorting can uncouple the genetic structure at neutral markers from the colonization history of populations. Here, we demonstrate multiple origins within ecotypes of an Australian wildflower, Senecio lautus. We observed strong genetic structure as well as phylogenetic clustering by geography and show that this is unlikely due to gene flow between parapatric ecotypes, which was surprisingly low. We further confirm this analytically by demonstrating that phylogenetic distortion due to gene flow often requires higher levels of migration than those observed in S. lautus. Our results imply that selection can repeatedly create similar phenotypes despite the perceived homogenizing effects of gene flow.     

Experimental evidence for reduced hybrid viability between dwarf and normal ecotypes of lake whitefish (Coregonus clupeaformis Mitchill)

Forces driving the evolution of reproductive isolation among natural populations, as well as the mechanisms involved to maintain it, are still poorly understood. Because sympatric fish ecotypes mainly differ in phenotypic traits associated with occupying distinct trophic niches, it is generally believed that reproductive isolation is mainly driven by ecological divergent selection, excluding genome incompatibility as a basis for postmating isolation. We did cross experiments between dwarf and normal ecotypes of lake whitefish (Coregonus clupeaformis Mitchill) originating from distinct glacial refugia to test the hypothesis that their geographical isolation during the Pleistocene may have led to sufficient genetic divergence for the development of reproductive isolation between them before their secondary contact. Similar fertilization success in pure and hybrid crosses indicated the absence of gametic incompatibility between the two ecotypes. In contrast, daily embryonic mortality rates were 2.4–4.7 times higher in reciprocal hybrid crosses compared to pure crosses, which supports our working hypothesis. These results, along with previous morphological and population genetic studies, indicate that both genetic and ecological mechanisms may jointly act to promote speciation among northern freshwater fish ecotypes.     

Paleo-population genetics

Two levels of population-genetic problems can be distinguished: (1) Distribution and population differences of monofactorial characters. In this connection, prehistoric physical anthropology is still very poor. (2) The study of processes which change the genetic structure of population. In this field also polyfactorial characters are important and may be used for analysis. Metric-morphological differentiations between and within skeletal populations are able to point at the following population genetic processes: migration and population mixture; genetic isolation and its effects; selection; social assortment, social stratification and assortative mating.     

Eco-Evolutionary Processes Generating Diversity Among Bottlenose Dolphin, <Emphasis Type="Italic">Tursiops truncatus</Emphasis>, Populations off Baja California,Mexico

For highly mobile species that nevertheless show fine-scale patterns of population genetic structure, the relevant evolutionary mechanisms determining structure remain poorly understood. The bottlenose dolphin (Tursiops truncatus) is one such species, exhibiting complex patterns of genetic structure associated with local habitat dependence in various geographic regions. Here we studied bottlenose dolphin populations in the Gulf of California and Pacific Ocean off Baja California where habitat is highly structured to test associations between ecology, habitat dependence and genetic differentiation. We investigated population structure at a fine geographic scale using both stable isotope analysis (to assess feeding ecology) and molecular genetic markers (to assess population structure). Our results show that there are at least two factors affecting population structure for both genetics and feeding ecology (as indicated by stable isotope profiles). On the one hand there is a signal for the differentiation of individuals by ecotype, one foraging more offshore than the other. At the same time, there is differentiation between the Gulf of California and the west coast of Baja California, meaning that for example, nearshore ecotypes were both genetically and isotopically differentiated either side of the peninsula. We discuss these data in the context of similar studies showing fine-scale population structure for delphinid species in coastal waters, and consider possible evolutionary mechanisms.     

Simple foraging rules in competitive environments can generate socially structured populations

Social vertebrates commonly form foraging groups whose members repeatedly interact with one another and are often genetically related. Many species also exhibit within‐population specializations, which can range from preferences to forage in particular areas through to specializing on the type of prey they catch. However, within‐population structure in foraging groups, behavioral homogeneity in foraging behavior, and relatedness could be outcomes of behavioral interactions rather than underlying drivers. We present a simple process by which grouping among foragers emerges and is maintained across generations. We introduce agent‐based models to investigate (1) whether a simple rule (keep foraging with the same individuals when you were successful) leads to stable social community structure, and (2) whether this structure is robust to demographic changes and becomes kin‐structured over time. We find the rapid emergence of kin‐structured populations and the presence of foraging groups that control, or specialize on, a particular food resource. This pattern is strongest in small populations, mirroring empirical observations. Our results suggest that group stability can emerge as a product of network self‐organization and, in doing so, may provide the necessary conditions for the evolution of more sophisticated processes, such as social learning. This taxonomically general social process has implications for our understanding of the links between population, genetic, and social structures.     

Population history and genetic structure of a circumpolar species: the arctic fox

The circumpolar arctic fox Alopex lagopus thrives in cold climates and has a high migration rate involving long-distance movements. Thus, it differs from many temperate taxa that were subjected to cyclical restriction in glacial refugia during the Ice Ages. We investigated population history and genetic structure through mitochondrial control region variation in 191 arctic foxes from throughout the arctic. Several haplotypes had a Holarctic distribution and no phylogeographical structure was found. Furthermore, there was no difference in haplotype diversity between populations inhabiting previously glaciated and unglaciated regions. This suggests current gene flow among the studied populations, with the exception of those in Iceland, which is surrounded by year-round open water. Arctic foxes have often been separated into two ecotypes: 'lemming' and 'coastal'. An analysis of molecular variance suggested particularly high gene flow among populations of the 'lemming' ecotype. This could be explained by their higher migration rate and reduced fitness in migrants between ecotypes. A mismatch analysis indicated a sudden expansion in population size around 118 000 BP, which coincides with the last interglacial. We propose that glacial cycles affected the arctic fox in a way opposite to their effect on temperate species, with interglacials leading to short-term isolation in northern refugia.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 79–89.     

Spatial arrangement and genetic structure in Gentianella aspera in a regional, local, and temporal context

Gentianella aspera is a biennial plant of various nutrient-poor grasslands that has become rare in the landscapes outside the Alps of eastern Austria. Using AFLP fingerprinting we investigated: (1) effects of spatial structure on genetic structure in a large vineyard population that is confined to the embankments separating the grapevines; (2) temporal variation in genetic diversity and structure in this population; (3) relationships with other populations in a regional context. On the regional scale, moderate isolation by distance among populations was revealed by a Mantel test. Bayesian analysis of population structure indicated three spatially distinct gene pools and an additional one within the vineyard population. Within this population, spatial autocorrelation analysis revealed a positive correlation between genetic and spatial distance up to 50 m. Patterns found by PCoA were not in line with a priori defined subpopulations and indicated substantial gene flow across embankments. AMOVA revealed low differentiation among both the subpopulations that were found on the linear embankments and among two local groups of these subpopulations. We found, however, striking differences in the among-group variation between the 2 years, i.e., between two local groups within the generations and between those groups among generations. This was due to the highly variable larger group of the younger generation, in which an additional gene pool was identified by Bayesian analysis of population structure. Based on these results we discuss scenarios of local and regional dynamics within and among G. aspera populations.     

Genetic structure and differentiation of <Emphasis Type="Italic">Oryza sativa</Emphasis> L. in China revealed by microsatellites

China is one of the largest centers of genetic diversity of Oryza sativa L. in the world. Using a genetically representative primary core collection of 3,024 rice landraces in China, we analyzed the genetic structure and intraspecific differentiation of O. sativa, and the directional evolution of SSR. The genetic structure was investigated by model-based structure analysis and construction of neighbor-joining phylogenetic tree. Comparison between genetic structure and predefined populations according to Ting’s taxonomic system revealed a hierarchical genetic structure: two distinct subspecies, each with three ecotypes and different numbers of geo-ecogroups within each ecotype. Two subspecies evidently resulted from adaptation to different environments. The different cropping systems imposed on the subspecies led to further differentiation, but the variation within each subspecies resulted from different causes. Indica, under tropical-like or lowland-like environments, exhibited clear differentiation among seasonal ecotypes, but not among soil-watery ecotypes; and japonica showed clear differences between soil water regime ecotypes, but not among seasonal ecotypes. Chinese cultivated rice took on evident directional evolution in microsatellite allele size at several aspects, such as subspecies and geographical populations. Japonica has smaller allele sizes than indica, and this may partly be the result of their different domestication times. Allele size was also negatively correlated with latitude and altitude, and this may be interpreted by different mutation rates, selection pressures, and population size effects under different environments and cropping systems.     

Fine-scale genetic structure and dispersal in the common vole (Microtus arvalis)

The genetic structure and demography of local populations is tightly linked to the rate and scale of dispersal. Dispersal parameters are notoriously difficult to determine in the field, and remain often completely unknown for smaller organisms. In this study, we investigate spatial and temporal genetic structure in relation to dispersal patterns among local populations of the probably most abundant European mammals, the common vole (Microtus arvalis). Voles were studied in six natural populations at distances of 0.4-2.5 km in three different seasons (fall, spring, summer) corresponding to different life-history stages. Field observations provided no direct evidence for movements of individuals between populations. The analysis of 10 microsatellite markers revealed a persistent overall genetic structure among populations of 2.9%, 2.5% and 3% FST in the respective season. Pairwise comparisons showed that even the closest populations were significantly differentiated from each other in each season, but there was no evidence for temporal differentiation within populations or isolation by distance among populations. Despite significant genetic structure, assignment analyses identified a relatively high proportion of individuals as being immigrants for the population where they were captured. The immigration rate was not significantly lower for females than for males. We suggest that a generally low and sex-dependent effective dispersal rate as the consequence of only few immigrants reproducing successfully in the new populations together with the social structure within populations may explain the maintenance of genetic differentiation among populations despite migration.     

Genetic and linguistic affinities between human populations in Eurasia and West Africa

This study examines the relationship between genetic distance and linguistic affiliation for five regional sets of populations from Eurasia and West Africa. Human genetic and linguistic diversity have been proposed to be generally correlated, either through a direct link, whereby linguistic and genetic affiliations reflect the same past population processes, or an indirect one, where the evolution of the two types of diversity is independent but conditioned by the same geographical factors. By controlling for proximity, indirect correlations due to common geography are eliminated, and any residual relationships found are likely to reflect common linguistic-genetic processes. Clear relationships between genetic distances and linguistic relatedness are detectable in Europe and East and Central Asia, but not in the Middle East, Southeast Asia, or West Africa. We suggest that linguistic and genetic affiliations will only be correlated under specific conditions, such as where there have been large-scale demic diffusions in the last few thousand years, and relative sedentism in the subsequent period.