Fine-scale genetic population structure in a mobile marine mammal: inshore bottlenose dolphins in Moreton Bay, Australia

Highly mobile marine species in areas with no obvious geographic barriers are expected to show low levels of genetic differentiation. However, small‐scale variation in habitat may lead to resource polymorphisms and drive local differentiation by adaptive divergence. Using nuclear microsatellite genotyping at 20 loci, and mitochondrial control region sequencing, we investigated fine‐scale population structuring of inshore bottlenose dolphins (Tursiops aduncus) inhabiting a range of habitats in and around Moreton Bay, Australia. Bayesian structure analysis identified two genetic clusters within Moreton Bay, with evidence of admixture between them (F_ST = 0.05, P = 0.001). There was only weak isolation by distance but one cluster of dolphins was more likely to be found in shallow southern areas and the other in the deeper waters of the central northern bay. In further analysis removing admixed individuals, southern dolphins appeared genetically restricted with lower levels of variation (AR = 3.252, π = 0.003) and high mean relatedness (r = 0.239) between individuals. In contrast, northern dolphins were more diverse (AR = 4.850, π = 0.009) and were mixing with a group of dolphins outside the bay (microsatellite‐based STRUCTURE analysis), which appears to have historically been distinct from the bay dolphins (mtDNA Φ_ST = 0.272, P < 0.001). This study demonstrates the ability of genetic techniques to expose fine‐scale patterns of population structure and explore their origins and mechanisms. A complex variety of inter‐related factors including local habitat variation, differential resource use, social behaviour and learning, and anthropogenic disturbances are likely to have played a role in driving fine‐scale population structure among bottlenose dolphins in Moreton Bay.     

Individual-based analysis opens new insights into understanding population structure and animal behaviour

Studying the movement of individuals in the wild has always been a challenge in ecology. However, estimating such movement is essential in life sciences as it is the base-line for evaluating connectivity, a major component in developing management and conservation plans. Furthermore, movement, or migration, is an essential parameter in population genetics, as it directly affects genetic differentiation. The development of highly variable markers has allowed genetic discrimination between individuals within populations and at larger scales, and the availability of high-throughput technologies means that many samples and hence many individuals can be screened. These advances mean that we can now use genetic identification for tracking individuals, and hence follow both survival and reproductive output through the life cycle. The paper by Morrissey & Ferguson (2011, this issue) is a demonstration of this new capability, as authors were able to infer the movement of salmonid fish initially captured as juveniles, and later as reproductively mature adults.     

Comparative analysis of landscape effects on spatial genetic structure of the big brown bat and one of its cimicid ectoparasites

Identification of landscape features that correlate with genetic structure permits understanding of factors that may influence gene flow in a species. Comparing effects of the landscape on a parasite and host provides potential insights into parasite‐host ecology. We compared fine‐scale spatial genetic structure between big brown bats (Eptesicus fuscus) and their cimicid ectoparasite (Cimex adjunctus; class Insecta) in the lower Great Lakes region of the United States, in an area of about 160,000 km². We genotyped 142 big brown bat and 55 C. adjunctus samples at eight and seven microsatellite loci, respectively, and inferred effects of various types of land cover on the genetic structure of each species. We found significant associations between several land cover types and genetic distance in both species, although different land cover types were influential in each. Our results suggest that even in a parasite that is almost entirely reliant on its hosts for dispersal, land cover can affect gene flow differently than in the hosts, depending on key ecological aspects of both species.     

Divergence with gene flow in a population of thermophilic bacteria: a potential role for spatially varying selection

A fundamental goal of evolutionary biology is to understand how ecological diversity arises and is maintained in natural populations. We have investigated the contributions of gene flow and divergent selection to the distribution of genetic variation in an ecologically differentiated population of a thermophilic cyanobacterium (Mastigocladus laminosus) found along the temperature gradient of a nitrogen‐limited stream in Yellowstone National Park. For most loci sampled, gene flow appears to be sufficient to prevent substantial genetic divergence. However, one locus (rfbC) exhibited a comparatively low migration rate as well as other signatures expected for a gene experiencing spatially varying selection, including an excess of common variants, an elevated level of polymorphism and extreme genetic differentiation along the gradient. rfbC is part of an expression island involved in the production of the polysaccharide component of the protective envelope of the heterocyst, the specialized nitrogen‐fixing cell of these bacteria. SNP genotyping in the vicinity of rfbC revealed a ~5‐kbp region including a gene content polymorphism that is tightly associated with environmental temperature and therefore likely contains the target of selection. Two genes have been deleted both in the predominant haplotype found in the downstream region of White Creek and in strains from other Yellowstone populations of M. laminosus, which may result in the production of heterocysts with different envelope properties. This study implicates spatially varying selection in the maintenance of variation related to thermal performance at White Creek despite on‐going or recent gene flow.     

Gene flow of Acanthaster planci (L.) in relation to ocean currents revealed by microsatellite analysis

Population outbreaks of the coral-eating starfish, Acanthaster planci , are hypothesized to spread to many localities in the Indo-Pacific Ocean through dispersal of planktonic larvae. To elucidate the gene flow of A. planci across the Indo-Pacific in relation to ocean currents and to test the larval dispersal hypothesis, the genetic structure among 23 samples over the Indo-Pacific was analysed using seven highly polymorphic microsatellite loci. The F -statistics and genetic admixture analysis detected genetically distinct groups in accordance with ocean current systems, that is, the Southeast African group (Kenya and Mayotte), the Northwestern Pacific group (the Philippines and Japan), Palau, the North Central Pacific group (Majuro and Pohnpei), the Great Barrier Reef, Fiji, and French Polynesia, with a large genetic break between the Indian and Pacific Oceans. A pattern of significant isolation by distance was observed among all samples ( P =  0.001, r  = 0.88, n  = 253, Mantel test), indicating restricted gene flow among the samples in accordance with geographical distances. The data also indicated strong gene flow within the Southeast African, Northwestern Pacific, and Great Barrier Reef groups. These results suggest that the western boundary currents have strong influence on gene flow of this species and may trigger secondary outbreaks.     

The role of genetic structure in the adaptive divergence of populations experiencing saltwater intrusion due to relative sea‐level rise

Saltwater intrusion into estuaries creates stressful conditions for nektonic species. Previous studies have shown that Gambusia affinis populations with exposure to saline environments develop genetic adaptations for increased survival during salinity stress. Here, we evaluate the genetic structure of G. affinis populations, previously shown to have adaptations for increased salinity tolerance, and determine the impact of selection and gene flow on structure of these populations. We found that gene flow was higher between populations experiencing different salinity regimes within an estuary than between similar marsh types in different estuaries, suggesting the development of saline‐tolerant phenotypes due to local adaptation. There was limited evidence of genetic structure along a salinity gradient, and only some of the genetic variation among sites was correlated with salinity. Our results suggest limited structure, combined with selection to saltwater intrusion, results in phenotypic divergence in spite of a lack of physical barriers to gene flow.     

Population genetic structure, gene flow and sex-biased dispersal in frillneck lizards (Chlamydosaurus kingii)

By using both mitochondrial and nuclear multiloci markers, we explored population genetic structure, gene flow and sex-specific dispersal of frillneck lizards ( Chlamydosaurus kingii ) sampled at three locations, separated by 10 to 50 km, in a homogenous savannah woodland in tropical Australia. Apart from a recombinant lizard, the mitochondrial analyses revealed two nonoverlapping haplotypes/populations, while the nuclear markers showed that the frillneck lizards represented three separate clusters/populations. Due to the small population size of the mtDNA, fixation may occur via founder effects and/or drift. We therefore suggest that either of these two processes, or a combination of the two, are the most likely causes of the discordant results obtained from the mitochondrial and the nuclear markers. In contrast to the nonoverlapping mitochondrial haplotypes, in 12 out of 74 lizards, mixed nuclear genotypes were observed, hence revealing a limited nuclear gene flow. Although gene flow should ultimately result in a blending of the populations, we propose that the distinct nuclear population structure is maintained by frequent fires resulting in local bottlenecks, and concomitant spatial separation of the frillneck lizard populations. Limited mark–recapture data and the difference in distribution of the mitochondrial and nuclear markers suggest that the mixed nuclear genotypes were caused by juvenile male-biased dispersal.     

Statistical methods in spatial genetics

The joint analysis of spatial and genetic data is rapidly becoming the norm in population genetics. More and more studies explicitly describe and quantify the spatial organization of genetic variation and try to relate it to underlying ecological processes. As it has become increasingly difficult to keep abreast with the latest methodological developments, we review the statistical toolbox available to analyse population genetic data in a spatially explicit framework. We mostly focus on statistical concepts but also discuss practical aspects of the analytical methods, highlighting not only the potential of various approaches but also methodological pitfalls.     

Limited gene dispersal and spatial genetic structure as stabilizing factors in an ant‐plant mutualism

Comparative studies of the population genetics of closely associated species are necessary to properly understand the evolution of these relationships because gene flow between populations affects the partners' evolutionary potential at the local scale. As a consequence (at least for antagonistic interactions), asymmetries in the strength of the genetic structures of the partner populations can result in one partner having a co‐evolutionary advantage. Here, we assess the population genetic structure of partners engaged in a species‐specific and obligatory mutualism: the Neotropical ant‐plant, Hirtella physophora, and its ant associate, Allomerus decemarticulatus. Although the ant cannot complete its life cycle elsewhere than on H. physophora and the plant cannot live for long without the protection provided by A. decemarticulatus, these species also have antagonistic interactions: the ants have been shown to benefit from castrating their host plant and the plant is able to retaliate against too virulent ant colonies. We found similar short dispersal distances for both partners, resulting in the local transmission of the association and, thus, inbred populations in which too virulent castrating ants face the risk of local extinction due to the absence of H. physophora offspring. On the other hand, we show that the plant populations probably experienced greater gene flow than did the ant populations, thus enhancing the evolutionary potential of the plants. We conclude that such levels of spatial structure in the partners' populations can increase the stability of the mutualistic relationship. Indeed, the local transmission of the association enables partial alignments of the partners' interests, and population connectivity allows the plant retaliation mechanisms to be locally adapted to the castration behaviour of their symbionts.     

Spatial and temporal population genetic structure of four northeastern Pacific littorinid gastropods: the effect of mode of larval development on variation at one mitochondrial and two nuclear DNA markers

We investigated the effect of development mode on the spatial and temporal population genetic structure of four littorinid gastropod species. Snails were collected from the same three sites on the west coast of Vancouver Island, Canada in 1997 and again in 2007. DNA sequences were obtained for one mitochondrial gene, cytochrome b ( Cyt b ), and for up to two nuclear genes, heat shock cognate 70 ( HSC70 ) and aminopeptidase N intron ( APN54 ). We found that the mean level of genetic diversity and long-term effective population sizes ( N _e) were significantly greater for two species, Littorina scutulata and L. plena , that had a planktotrophic larval stage than for two species, Littorina sitkana and L. subrotundata , that laid benthic egg masses which hatched directly into crawl-away juveniles. Predictably, two poorly dispersing species, L. sitkana and L. subrotundata , showed significant spatial genetic structure at an 11- to 65-km geographical scale that was not observed in the two planktotrophic species. Conversely, the two planktotrophic species had more temporal genetic structure over a 10-year interval than did the two direct-developing species and showed highly significant temporal structure for spatially pooled samples. The greater temporal genetic variation of the two planktotrophic species may have been caused by their high fecundity, high larval dispersal, and low but spatially correlated early survivorship. The sweepstakes-like reproductive success of the planktotrophic species could allow a few related females to populate hundreds of kilometres of coastline and may explain their substantially larger temporal genetic variance but lower spatial genetic variance relative to the direct-developing species.     

群体遗传结构中的基因流

群体遗传结构上的差异是遗传多样性的一种重要体现,对群体遗传结构的研究已有较久的历史,而其中的基因流研究近些年来越来越受到重视。它对群体遗传学、进化生物学、保护生物学、生态学有着极其重要的作用。虽然传统的群体遗传学能估测基因流大小,但它的精确性还有很大局限性。随着生物技术的进步,对基因流的研究逐渐向分子水平过渡,应用蛋白质电泳技术、分子标记技术(RAPD、RFLP、VNTR、ISSR、DNA测序等)方法对群体间基因流的流动水平进行了深入细致的研究。通过综述群体遗传结构的几种模式:陆岛模式、海岛模式、阶石模式、距离隔离模式、层次模式,以及在群体遗传结构的几种模式基础上的基因流的研究方法、作用、地位和近些年来研究者的研究成果,并指出了这些方法的局限性。     

Rainfall can explain adaptive phenotypic variation with high gene flow in the New Holland Honeyeater (Phylidonyris novaehollandiae)

Identifying environmentally driven changes in traits that serve an ecological function is essential for predicting evolutionary outcomes of climate change. We examined population genetic structure, sex‐specific dispersal patterns, and morphology in relation to rainfall patterns across an island and three peninsulas in South Australia. The study system was the New Holland Honeyeater (Phylidonyris novaehollandiae), a nectarivorous passerine that is a key pollinator species. We predicted that rainfall‐related mechanisms would be driving local adaptation of morphological traits, such that in areas of lower rainfall, where nectar is less available, more insectivorous traits – shorter, deeper bills, longer tarsi, and longer wings – would be favored. The study populations differed in phenotype across the Eyre, Yorke, and Fleurieu Peninsulas and Kangaroo Island despite high gene flow (single continuous population) and sex‐biased dispersal (males were philopatric and females dispersed). We tested the role of rainfall in shaping the observed phenotypic differences, and found strong support for our predicted relationships: birds in areas of higher rainfall had higher condition indices, as well as longer bill‐head length, deeper bills, and shorter tarsi. Bill depth in males in high‐rainfall sites showed signals of stabilizing selection, suggesting local adaptation. In addition to these local indications of selection, a global pattern of directional selection toward larger size for bill‐head length, bill‐nostril length, and wing length was also observed. We suggest this pattern may reflect an adaptive response to the relatively dry conditions that South Australia has experienced over the last decade. We conclude that rainfall has shaped aspects of phenology in P. novaehollandiae, both locally, with different patterns of stabilizing and directional selection, and globally, with evidence of adaptive divergence at a landscape scale.     

Meta‐analysis reveals lower genetic diversity in overfished populations

While population declines can drive the loss of genetic diversity under some circumstances, it has been unclear whether this loss is a general consequence of overharvest in highly abundant marine fishes. We compiled data from 11 049 loci across 140 species and found that allelic richness was lower in overfished populations within 9 of 12 genera and families. A multiple linear regression showed that allelic richness was on average 12% lower (P < 0.0001) in overharvested populations after accounting for the effects of body size, latitude and other factors. Heterozygosity was on average 2% lower (P = 0.030). Simulations confirmed that these patterns are consistent with a recent bottleneck in abundant species and also showed that our analysis likely underestimates the loss of rare alleles by a factor of two or three. This evidence suggests that overharvest drives the decay of genetic diversity across a wide range of marine fishes. Such reductions of genetic diversity in some of the world's most abundant species may lead to a long‐term impact of fishing on their evolutionary potential, particularly if abundance remains low and diversity continues to decay.     

These aren’t the loci you’e looking for: Principles of effective SNP filtering for molecular ecologists

Sequencing reduced‐representation libraries of restriction site‐associated DNA (RADseq) to identify single nucleotide polymorphisms (SNPs) is quickly becoming a standard methodology for molecular ecologists. Because of the scale of RADseq data sets, putative loci cannot be assessed individually, making the process of filtering noise and correctly identifying biologically meaningful signal more difficult. Artefacts introduced during library preparation and/or bioinformatic processing of SNP data can create patterns that are incorrectly interpreted as indicative of population structure or natural selection. Therefore, it is crucial to carefully consider types of errors that may be introduced during laboratory work and data processing, and how to minimize, detect and remove these errors. Here, we discuss issues inherent to RADseq methodologies that can result in artefacts during library preparation and locus reconstruction resulting in erroneous SNP calls and, ultimately, genotyping error. Further, we describe steps that can be implemented to create a rigorously filtered data set consisting of markers accurately representing independent loci and compare the effect of different combinations of filters on four RAD data sets. At last, we stress the importance of publishing raw sequence data along with final filtered data sets in addition to detailed documentation of filtering steps and quality control measures.     

Effects of social organization and elevation on spatial genetic structure in a montane ant

Studying patterns of population structure across the landscape sheds light on dispersal and demographic processes, which helps to inform conservation decisions. Here, we study how social organization and landscape factors affect spatial patterns of genetic differentiation in an ant species living in mountainous regions. Using genome‐wide SNP markers, we assess population structure in the Alpine silver ant, Formica selysi. This species has two social forms controlled by a supergene. The monogyne form has one queen per colony, while the polygyne form has multiple queens per colony. The two social forms co‐occur in the same populations. For both social forms, we found a strong pattern of isolation‐by‐distance across the Alps. Within regions, genetic differentiation between populations was weaker for the monogyne form than for the polygyne form. We suggest that this pattern is due to higher dispersal and effective population sizes in the monogyne form. In addition, we found stronger isolation‐by‐distance and lower genetic diversity in high elevation populations, compared to lowland populations, suggesting that gene flow between F. selysi populations in the Alps occurs mostly through riparian corridors along lowland valleys. Overall, this survey highlights the need to consider intraspecific polymorphisms when assessing population connectivity and calls for special attention to the conservation of lowland habitats in mountain regions.     

Landscape genetics and hierarchical genetic structure in Atlantic salmon: the interaction of gene flow and local adaptation

Disentangling evolutionary forces that may interact to determine the patterns of genetic differentiation within and among wild populations is a major challenge in evolutionary biology. The objective of this study was to assess the genetic structure and the potential influence of several ecological variables on the extent of genetic differentiation at multiple spatial scales in a widely distributed species, the Atlantic salmon, Salmo salar . A total of 2775 anadromous fish were sampled from 51 rivers along the North American Atlantic coast and were genotyped using 13 microsatellites. A Bayesian analysis clustered these populations into seven genetically and geographically distinct groups, characterized by different environmental and ecological factors, mainly temperature. These groups were also characterized by different extent of genetic differentiation among populations. Dispersal was relatively high and of the same magnitude within compared to among regional groups, which contrasted with the maintenance of a regional genetic structure. However, genetic differentiation was lower among populations exchanging similar rates of local as opposed to inter-regional migrants, over the same geographical scale. This raised the hypothesis that gene flow could be constrained by local adaptation at the regional scale. Both coastal distance and temperature regime were found to influence the observed genetic structure according to landscape genetic analyses. The influence of other factors such as latitude, river length and altitude, migration tactic, and stocking was not significant at any spatial scale. Overall, these results suggested that the interaction between gene flow and thermal regime adaptation mainly explained the hierarchical genetic structure observed among Atlantic salmon populations.     

Widespread hybridization and bidirectional introgression in sympatric species of coral reef fish

Coral reefs are highly diverse ecosystems, where numerous closely related species often coexist. How new species arise and are maintained in these high geneflow environments have been long‐standing conundrums. Hybridization and patterns of introgression between sympatric species provide a unique insight into the mechanisms of speciation and the maintenance of species boundaries. In this study, we investigate the extent of hybridization between two closely related species of coral reef fish: the common coral trout (Plectropomus leopardus) and the bar‐cheek coral trout (Plectropomus maculatus). Using a complementary set of 25 microsatellite loci, we distinguish pure genotype classes from first‐ and later‐generation hybrids, identifying 124 interspecific hybrids from a collection of 2,991 coral trout sampled in inshore and mid‐shelf reefs of the southern Great Barrier Reef. Hybrids were ubiquitous among reefs, fertile and spanned multiple generations suggesting both ecological and evolutionary processes are acting to maintain species barriers. We elaborate on these finding to investigate the extent of genomic introgression and admixture from 2,271 SNP loci recovered from a ddRAD library of pure and hybrid individuals. An analysis of genomic clines on recovered loci indicates that 261 SNP loci deviate from a model of neutral introgression, of which 132 indicate a pattern of introgression consistent with selection favouring both hybrid and parental genotypes. Our findings indicate genome‐wide, bidirectional introgression between two sympatric species of coral reef fishes and provide further support to a growing body of evidence for the role of hybridization in the evolution of coral reef fishes.     

Seascape genetics along environmental gradients in the Arabian Peninsula: insights from ddRAD sequencing of anemonefishes

Understanding the processes that shape patterns of genetic structure across space is a central aim of landscape genetics. However, it remains unclear how geographical features and environmental variables shape gene flow, particularly for marine species in large complex seascapes. Here, we evaluated the genomic composition of the two‐band anemonefish Amphiprion bicinctus across its entire geographical range in the Red Sea and Gulf of Aden, as well as its close relative, Amphiprion omanensis endemic to the southern coast of Oman. Both the Red Sea and the Arabian Sea are complex and environmentally heterogeneous marine systems that provide an ideal scenario to address these questions. Our findings confirm the presence of two genetic clusters previously reported for A. bicinctus in the Red Sea. Genetic structure analyses suggest a complex seascape configuration, with evidence of both isolation by distance (IBD) and isolation by environment (IBE). In addition to IBD and IBE, genetic structure among sites was best explained when two barriers to gene flow were also accounted for. One of these coincides with a strong oligotrophic–eutrophic gradient at around 16–20?N in the Red Sea. The other agrees with a historical bathymetric barrier at the straight of Bab al Mandab. Finally, these data support the presence of interspecific hybrids at an intermediate suture zone at Socotra and indicate complex patterns of genomic admixture in the Gulf of Aden with evidence of introgression between species. Our findings highlight the power of recent genomic approaches to resolve subtle patterns of gene flow in marine seascapes.     

Comparative landscape genetics reveals differential effects of environment on host and pathogen genetic structure in Tasmanian devils (Sarcophilus harrisii) and their transmissible tumour

Genetic structure in host species is often used to predict disease spread. However, host and pathogen genetic variation may be incongruent. Understanding landscape factors that have either concordant or divergent influence on host and pathogen genetic structure is crucial for wildlife disease management. Devil facial tumour disease (DFTD) was first observed in 1996 and has spread throughout almost the entire Tasmanian devil geographic range, causing dramatic population declines. Whereas DFTD is predominantly spread via biting among adults, devils typically disperse as juveniles, which experience low DFTD prevalence. Thus, we predicted little association between devil and tumour population structure and that environmental factors influencing gene flow differ between devils and tumours. We employed a comparative landscape genetics framework to test the influence of environmental factors on patterns of isolation by resistance (IBR) and isolation by environment (IBE) in devils and DFTD. Although we found evidence for broad‐scale costructuring between devils and tumours, we found no relationship between host and tumour individual genetic distances. Further, the factors driving the spatial distribution of genetic variation differed for each. Devils exhibited a strong IBR pattern driven by major roads, with no evidence of IBE. By contrast, tumours showed little evidence for IBR and a weak IBE pattern with respect to elevation in one of two tumour clusters we identify herein. Our results warrant caution when inferring pathogen spread using host population genetic structure and suggest that reliance on environmental barriers to host connectivity may be ineffective for managing the spread of wildlife diseases. Our findings demonstrate the utility of comparative landscape genetics for identifying differential factors driving host dispersal and pathogen transmission.     

The role of structural genomic variants in population differentiation and ecotype formation in Timema cristinae walking sticks

Theory predicts that structural genomic variants such as inversions can promote adaptive diversification and speciation. Despite increasing empirical evidence that adaptive divergence can be triggered by one or a few large inversions, the degree to which widespread genomic regions under divergent selection are associated with structural variants remains unclear. Here we test for an association between structural variants and genomic regions that underlie parallel host‐plant‐associated ecotype formation in Timema cristinae stick insects. Using mate‐pair resequencing of 20 new whole genomes we find that moderately sized structural variants such as inversions, deletions and duplications are widespread across the genome, being retained as standing variation within and among populations. Using 160 previously published, standard‐orientation whole genome sequences we find little to no evidence that the DNA sequences within inversions exhibit accentuated differentiation between ecotypes. In contrast, a formerly described large region of reduced recombination that harbours genes controlling colour‐pattern exhibits evidence for accentuated differentiation between ecotypes, which is consistent with differences in the frequency of colour‐pattern morphs between host‐associated ecotypes. Our results suggest that some types of structural variants (e.g., large inversions) are more likely to underlie adaptive divergence than others, and that structural variants are not required for subtle yet genome‐wide genetic differentiation with gene flow.