Small‐ and large‐scale heterogeneity in genetic variation across the collard flycatcher genome: implications for estimating genetic diversity in nonmodel organisms

Population genetic studies in nonmodel organisms are often hampered by a lack of reference genomes that are essential for whole‐genome resequencing. In the light of this, genotyping methods have been developed to effectively eliminate the need for a reference genome, such as genotyping by sequencing or restriction site‐associated DNA sequencing (RAD‐seq). However, what remains relatively poorly studied is how accurately these methods capture both average and variation in genetic diversity across an organism's genome. In this issue of Molecular Ecology Resources, Dutoit et al. (2016) use whole‐genome resequencing data from the collard flycatcher to assess what factors drive heterogeneity in nucleotide diversity across the genome. Using these data, they then simulate how well different sequencing designs, including RAD sequencing, could capture most of the variation in genetic diversity. They conclude that for evolutionary and conservation‐related studies focused on the estimating genomic diversity, researchers should emphasize the number of loci analysed over the number of individuals sequenced.     

Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus

The European green crab Carcinus maenas is one of the world's most successful aquatic invaders, having established populations on every continent with temperate shores. Here we describe patterns of genetic diversity across both the native and introduced ranges of C. maenas and its sister species, C. aestuarii, including all known non‐native populations. The global data set includes sequences from the mitochondrial cytochrome c oxidase subunit I gene, as well as multilocus genotype data from nine polymorphic nuclear microsatellite loci. Combined phylogeographic and population genetic analyses clarify the global colonization history of C. maenas, providing evidence of multiple invasions to Atlantic North America and South Africa, secondary invasions to the northeastern Pacific, Tasmania, and Argentina, and a strong likelihood of C. maenas × C. aestuarii hybrids in South Africa and Japan. Successful C. maenas invasions vary broadly in the degree to which they retain genetic diversity, although populations with the least variation typically derive from secondary invasions or from introductions that occurred more than 100 years ago.     

Ex situ cultivation affects genetic structure and diversity in arable plants

Worldwide, botanical gardens cultivate around 80,000 taxa, corresponding to approximately one‐quarter of all vascular plants. Most cultivated taxa are, however, held in a small number of collections, and mostly only in small populations. Lack of genetic exchange and stochastic processes in small populations make them susceptible to detrimental genetic effects, which should be most severe in annual species, as sowing cycles are often short. In order to assess whether ex situ cultivation affects genetic diversity of annuals, five annual arable species with similar breeding systems were assessed with 42 in situ populations being compared to 20 ex situ populations using a random amplified polymorphic DNA (RAPD) analysis approach. Population sizes tended to be lower under ex situ cultivation and levels of genetic diversity also tended to be lower in four of the five species, with differences being significant in only two. Ex situ populations showed incomplete representation of alleles found in the wild. The duration of cultivation did not indicate any effect on genetic diversity. This implies that cultivation strategies resulted in different genetic structures in the garden populations. Although not unequivocally pronounced, differences nonetheless imply that conservation strategies in the involved gardens may need improvement. One option is cold storage of seeds, a practice that is not currently followed in the studied ex situ collections. This may reflect that the respective gardens focus on displaying living plant populations.     

Reconstructing demographic events from population genetic data: the introduction of bumblebees to New Zealand

Four British bumblebee species (Bombus terrestris, Bombus hortorum, Bombus ruderatus and Bombus subterraneus) became established in New Zealand following their introduction at the turn of the last century. Of these, two remain common in the United Kingdom (B. terrestris and B. hortorum), whilst two (B. ruderatus and B. subterraneus) have undergone marked declines, the latter being declared extinct in 2000. The presence of these bumblebees in New Zealand provides an unique system in which four related species have been isolated from their source population for over 100 years, providing a rare opportunity to examine the impacts of an initial bottleneck and introduction to a novel environment on their population genetics. We used microsatellite markers to compare modern populations of B. terrestris, B. hortorum and B. ruderatus in the United Kingdom and New Zealand and to compare museum specimens of British B. subterraneus with the current New Zealand population. We used approximate Bayesian computation to estimate demographic parameters of the introduction history, notably to estimate the number of founders involved in the initial introduction. Species-specific patterns derived from genetic analysis were consistent with the predictions based on the presumed history of these populations; demographic events have left a marked genetic signature on all four species. Approximate Bayesian analyses suggest that the New Zealand population of B. subterraneus may have been founded by as few as two individuals, giving rise to low genetic diversity and marked genetic divergence from the (now extinct) UK population.     

The impact of translocations on neutral and functional genetic diversity within and among populations of the Seychelles warbler

Translocations are an increasingly common tool in conservation. The maintenance of genetic diversity through translocation is critical for both the short‐ and long‐term persistence of populations and species. However, the relative spatio‐temporal impacts of translocations on neutral and functional genetic diversity, and how this affects genetic structure among the conserved populations overall, have received little investigation. We compared the impact of translocating different numbers of founders on both microsatellite and major histocompatibility complex (MHC) class I diversity over a 23‐year period in the Seychelles warbler (Acrocephalus sechellensis). We found low and stable microsatellite and MHC diversity in the source population and evidence for only a limited loss of either type of diversity in the four new populations. However, we found evidence of significant, but low to moderate, genetic differentiation between populations, with those populations established with fewer founders clustering separately. Stochastic genetic capture (as opposed to subsequent drift) was the main determinant of translocated population diversity. Furthermore, a strong correlation between microsatellite and MHC differentiation suggested that neutral processes outweighed selection in shaping MHC diversity in the new populations. These data provide important insights into how to optimize the use of translocation as a conservation tool.     

Connections between species diversity and genetic diversity

Species diversity and genetic diversity remain the nearly exclusive domains of community ecology and population genetics, respectively, despite repeated recognition in the literature over the past 30 years of close parallels between these two levels of diversity. Species diversity within communities and genetic diversity within populations are hypothesized to co‐vary in space or time because of locality characteristics that influence the two levels of diversity via parallel processes, or because of direct effects of one level of diversity on the other via several different mechanisms. Here, we draw on a wide range of studies in ecology and evolution to examine the theoretical underpinnings of these hypotheses, review relevant empirical literature, and outline an agenda for future research. The plausibility of species diversity–genetic diversity relationships is supported by a variety of theoretical and empirical studies, and several recent studies provide direct, though preliminary support. Focusing on potential connections between species diversity and genetic diversity complements other approaches to synthesis at the ecology–evolution interface, and should contribute to conceptual unification of biodiversity research at the levels of genes and species.     

The role of global trade and transport network topology in the human‐mediated dispersal of alien species

More people and goods are moving further and more frequently via many different trade and transport networks under current trends of globalisation. These networks can play a major role in the unintended introduction of exotic species to new locations. With the continuing rise in global trade, more research attention is being focused on the role of networks in the spread of invasive species. This represents an emerging field of research in invasion science and the substantial knowledge being generated within other disciplines can provide ecologists with new tools with which to study invasions. For the first time, we synthesise studies from several perspectives, approaches and disciplines to derive the fundamental characteristics of network topology determining the likelihood of spread of organisms via trade and transport networks. These characteristics can be used to identify critical points of vulnerability within these networks and enable the development of more effective strategies to prevent invasions.     

Life on the margin: genetic isolation and diversity loss in a peripheral marine ecosystem, the Baltic Sea

Marginal populations are often isolated and under extreme selection pressures resulting in anomalous genetics. Consequently, ecosystems that are geographically and ecologically marginal might have a large share of genetically atypical populations, in need of particular concern in management of these ecosystems. To test this prediction, we analysed genetic data from 29 species inhabiting the low saline Baltic Sea, a geographically and ecologically marginal ecosystem. On average Baltic populations had lost genetic diversity compared to Atlantic populations: a pattern unrelated to dispersal capacity, generation time of species and taxonomic group of organism, but strongly related to type of genetic marker (mitochondrial DNA loci had lost c. 50% diversity, and nuclear loci 10%). Analyses of genetic isolation by geographic distance revealed clinal patterns of differentiation between Baltic and Atlantic regions. For a majority of species, clines were sigmoid with a sharp slope around the Baltic Sea entrance, indicating impeded gene flows between Baltic and Atlantic populations. Some species showed signs of allele frequencies being perturbed at the edge of their distribution inside the Baltic Sea. Despite the short geological history of the Baltic Sea (8000 years), populations inhabiting the Baltic have evolved substantially different from Atlantic populations, probably as a consequence of isolation and bottlenecks, as well as selection on adaptive traits. In addition, the Baltic Sea also acts a refuge for unique evolutionary lineages. This marginal ecosystem is thus vulnerable but also exceedingly valuable, housing unique genes, genotypes and populations that constitute an important genetic resource for management and conservation.     

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.     

Non‐genetic diversity modulates population performance

Biological functions are typically performed by groups of cells that express predominantly the same genes, yet display a continuum of phenotypes. While it is known how one genotype can generate such non‐genetic diversity, it remains unclear how different phenotypes contribute to the performance of biological function at the population level. We developed a microfluidic device to simultaneously measure the phenotype and chemotactic performance of tens of thousands of individual, freely swimming Escherichia coli as they climbed a gradient of attractant. We discovered that spatial structure spontaneously emerged from initially well‐mixed wild‐type populations due to non‐genetic diversity. By manipulating the expression of key chemotaxis proteins, we established a causal relationship between protein expression, non‐genetic diversity, and performance that was theoretically predicted. This approach generated a complete phenotype‐to‐performance map, in which we found a nonlinear regime. We used this map to demonstrate how changing the shape of a phenotypic distribution can have as large of an effect on collective performance as changing the mean phenotype, suggesting that selection could act on both during the process of adaptation.     

Conservation priorities of genetic diversity in domesticated metapopulations: a study in taurine cattle breeds

We estimated neutral diversity of 21 European cattle breeds with 105 microsatellites. Nine of them resembled unselected Balkan Buša strains with diffuse breeding barriers and the 12 others were strongly differentiated, isolated breeds. Because of the impact of neutral genetic diversity on long-term population adaptive capacity, we discuss the long-term outcome of different conservation priorities in a subdivided metapopulation of the investigated cattle breeds. The optimal contribution to a pool of total genetic diversity allocated more than 95% of long-term relevant neutral diversity to virtually unselected strains of the Balkan Buša, while the maximization of total variance preferred inbred breeds. Current artificial selection methods, such as genomic selection sped up and a recovery of underestimated traits becomes quickly impossible. We emphasize that currently neutral and even deleterious alleles might be required for future genotypes in sustainable and efficient livestock breeding and production systems of a 21st century. We provide cumulative evidences that long-term survival relies on genetic complexity and complexity relies on allelic diversity. Our results suggest that virtually unselected, nonuniform strains harbor a crucial proportion of neutral diversity and should be conserved with high global priority. As one example, we suggest a cooperative maintenance of the nondifferentiated, highly fragmented, and fast vanishing metapopulation of Balkan Buša.     

Anthropogenic fragmentation may not alter pre‐existing patterns of genetic diversity and differentiation in perennial shrubs

Many plant species have pollination and seed dispersal systems and evolutionary histories that have produced strong genetic structuring. These genetic patterns may be consistent with expectations following recent anthropogenic fragmentation, making it difficult to detect fragmentation effects if no prefragmentation genetic data are available. We used microsatellite markers to investigate whether severe habitat fragmentation may have affected the structure and diversity of populations of the endangered Australian bird‐pollinated shrub Grevillea caleyi R.Br., by comparing current patterns of genetic structure and diversity with those of the closely related G. longifolia R.Br. that has a similar life history but has not experienced anthropogenic fragmentation. Grevillea caleyi and G. longifolia showed similar and substantial population subdivision at all spatial levels (global F′_ST = 0.615 and 0.454; S_p = 0.039 and 0.066), marked isolation by distance and large heterozygous deficiencies. These characteristics suggest long‐term effects of inbreeding in self‐compatible species that have poor seed dispersal, limited connectivity via pollen flow and undergo population bottlenecks because of periodic fires. Highly structured allele size distributions, most notably in G. caleyi, imply historical processes of drift and mutation were important in isolated subpopulations. Genetic diversity did not vary with population size but was lower in more isolated populations for both species. Through this comparison, we reject the hypothesis that anthropogenic fragmentation has impacted substantially on the genetic composition or structure of G. caleyi populations. Our results suggest that highly self‐compatible species with limited dispersal may be relatively resilient to the genetic changes predicted to follow habitat fragmentation.     

bottlesim: a bottleneck simulation program for long‐lived species with overlapping generations

Population bottlenecks reduce genetic diversity and thus cause great concern in conservation biology. Previous theoretical studies often assume discrete generations in projecting declines in genetic diversity caused by bottlenecks. This assumption creates complexities when applying the models to long‐lived species with overlapping generations. bottlesim is a program for simulating bottlenecks to estimate the impact on genetic diversity; the novelties include an overlapping‐generation model, a wide range of reproductive systems, and flexible population size settings. With these features, bottlesim will be a useful tool for estimating the genetic consequences of bottlenecks, evaluating conservation plans, and performing power analysis.     

Contrasting effects of long distance seed dispersal on genetic diversity during range expansion

Currently many attempts are made to reconstruct the colonization history of plant species after the last ice age. A surprising finding is that during the colonization phase genetic diversity did not decrease as much as expected. In this paper we examine whether long distance seed dispersal events could play a role in the unexpected maintenance of genetic diversity during range expansion. This study is based on simulations carried out with a maternally inherited haploid locus using a cellular automaton. The simulations reveal a close relationship between the frequency of long distance seed dispersal events and the amount of genetic diversity preserved during colonization. In particular, when the colonized region is narrow, a complete loss of genetic diversity results from the occurrence of very rare long distance dispersal (LDD) events. We call this phenomenon the 'embolism effect'. However, slightly higher rates of LDD events reverse this effect, up to the point that diversity is better preserved than in a pure diffusion model. This phenomenon is linked to the reorganization of the genetic structure during colonization and is called the 'reshuffling effect'.     

Microsatellite analysis reveals high genetic diversity but low genetic structure in Ethiopian indigenous cattle populations

Ethiopian cattle are under threat from uncontrolled mating practices and are at high risk of becoming genetically homogeneous. Therefore, to evaluate genetic diversity, population structure and degree of admixture, 30 microsatellite markers were genotyped using 351 DNA samples from 10 Ethiopian cattle populations and the Holstein breed. The mean number of alleles per cattle population ranged from 6.93 ± 2.12 in Sheko to 7.50 ± 2.35 in Adwa. The mean observed and expected heterozygosities were 0.674 ± 0.015 and 0.726 ± 0.019 respectively. Ethiopian cattle populations have maintained a high level of within-population genetic differentiation (98.7%), the remainder being accounted for by differentiation among populations (1.3%). A highly significant deficiency in heterozygotes was detected within populations ( F _IS = 0.071; P  <   0.001) and total inbreeding ( F _IT = 0.083; P  <   0.001). The study populations were highly admixed but distinct from pure Bos taurus and Bos indicus breeds. The various levels of admixture and high genetic diversity make Ethiopian cattle populations suitable for future genetic improvement and utilization under a wide range of agro-ecologies in Ethiopia.     

Long-term survival despite low genetic diversity in the critically endangered Madagascar fish-eagle

The critically endangered Madagascar fish-eagle ( Haliaeetus vociferoides ) is considered to be one of the rarest birds of prey globally and at significant risk of extinction. In the most recent census, only 222 adult individuals were recorded with an estimated total breeding population of no more than 100–120 pairs. Here, levels of Madagascar fish-eagle population genetic diversity based on 47 microsatellite loci were compared with its sister species, the African fish-eagle ( Haliaeetus vocifer ), and 16 of these loci were also characterized in the white-tailed eagle ( Haliaeetus albicilla ) and the bald eagle ( Haliaeetus leucocephalus ). Overall, extremely low genetic diversity was observed in the Madagascar fish-eagle compared to other surveyed Haliaeetus species. Determining whether this low diversity is the result of a recent bottleneck or a more historic event has important implications for their conservation. Using a Bayesian coalescent-based method, we show that Madagascar fish-eagles have maintained a small effective population size for hundreds to thousands of years and that its low level of neutral genetic diversity is not the result of a recent bottleneck. Therefore, efforts made to prevent Madagascar fish-eagle extinction should place high priority on maintenance of habitat requirements and reducing direct and indirect human persecution. Given the current rate of deforestation in Madagascar, we further recommend that the population be expanded to occupy a larger geographical distribution. This will help the population persist when exposed to stochastic factors (e.g. climate and disease) that may threaten a species consisting of only 200 adult individuals while inhabiting a rapidly changing landscape.     

Seed bank influences on genetic diversity in the rare annual Clarkia springvillensis (Onagraceae)

The potential for seed banks to significantly affect the genetic structure of populations was recognized nearly two decades ago. However, there has been little empirical work that examines the problem. In this study, we explore the possibility that the seed bank of a rare annual, Clarkia springvillensis, could act as a buffer against the genetic consequences of small population size. We examined the adult and seed bank cohort in three natural populations. The seed bank was surveyed by collecting soil cores twice during the growing season: postgermination and post seed set. The genetic constitution of the adults and seed bank cohort was determined by examining eight polymorphic isozyme loci via starch gel electrophoresis. The total genetic diversity in the seed bank (Ht = 0.355) was significantly higher than in the adults (Ht = 0.260). Additionally, Fst estimates of genetic differentiation among populations showed significantly less differentiation among population seed banks (Fst = 0.008) than among adults (Fst = 0.045). These results are in agreement with the expectation that seed banks would act to maintain genetic diversity in populations as well as have the effect of slowing differentiation of populations.