The contributions of distinct populations to annual harvests provide key insights to conservation, especially in migratory species that return to specific reproductive areas. In this context, genetic stock identification (GSI) requires reference samples from source populations to assign harvested individuals, yet sampling might be challenging as reproductive areas could be remote and/or unknown. To investigate intraspecific variation in walleye (Sander vitreus) populations harvested in two large lakes in northern Quebec, we used genotyping-by-sequencing data to develop a panel of 303 filtered single-nucleotide polymorphisms. We then genotyped 1465 fish and assessed individual migration distances from GPS coordinates of capture locations. Samples were assigned to a source population using two methods, one requiring allele frequencies of known populations (RUBIAS) and the other without prior knowledge (STRUCTURE). Individual assignments to a known population reached 93% consistency between both methods in the main lake where we identified all five major source populations. However, the analyses also revealed up to three small unsampled populations. Furthermore, populations were characterised by large differences in average migration distance. In contrast, assignment consistency reached 99% in the neighbouring lake and walleye were assigned with high confidence to two populations having a similar distribution throughout the lake. The complex population structure and migration patterns in the main lake suggest a more heterogeneous habitat and thus, greater potential for local adaptation. This study highlights how combining analytical approaches can inform the robustness of GSI results in a given system and detect intraspecific diversity and complexity relevant for conservation.
Intraspecific variation is important for species’ long-term persistence in changing environments. Conservation strategies targeting intraspecific variation often rely on the identification of management or policy units below the species level based on biological differences among populations. To identify management units, this paper examines intraspecific divergence of Lake Trout (Salvelinus namaycush) in Great Slave Lake (GSL), Canada, using low-coverage whole-genome sequencing data. Specifically, we evaluate genetic differentiation and assess the relationship with morphological, mitochondrial, and putatively adaptive divergence. We show that at least three and up to five genetically distinct Lake Trout populations co-occur in GSL and exhibit differences in spatial distribution and body size, with signatures of selection. However, admixture was widespread (60% of the fish) and population structure was shallow (average FST = 0.022). These findings highlight that, even in the era of whole genome sequencing, identifying discrete management units to implement conservation efforts and policy can remain challenging in systems where gene flow among genetically and ecologically distinct populations is ubiquitous. To give more recognition to this complexity, management efforts should also focus on the area where adaptive variation is evident, and evolutionary acts are at play, to better protect species’ resilience and adaptive potential in some natural systems.
Single nucleotide polymorphism (SNP) panels are powerful tools for assessing the genetic population structure and dispersal of fishes and can enhance management practices for commercial, recreational and subsistence mixed-stock fisheries. Arctic Char (Salvelinus alpinus), Brook Trout (Salvelinus fontinalis) and Lake Whitefish (Coregonus clupeaformis) are among the most harvested and consumed fish species in Northern Indigenous communities in Canada, contributing significantly to food security, culture, tradition and economy. However, genetic resources supporting Indigenous fisheries have not been widely accessible to northern communities (e.g. Inuit, Cree, Dene). Here, we developed Genotyping-in-Thousands by sequencing (GT-seq) panels for population assignment and mixed-stock analyses of three salmonids, to support fisheries stewardship or co-management in Northern Canada. Using low-coverage Whole Genome Sequencing data from 418 individuals across source populations in Cambridge Bay (Nunavut), Great Slave Lake (Northwest Territories), James Bay (Québec) and Mistassini Lake (Québec), we developed a bioinformatic SNP filtering workflow to select informative SNP markers from genotype likelihoods. These markers were then used to design GT-seq panels, thus enabling high-throughput genotyping for these species. The three GT-seq panels yielded an average of 413 autosomal loci and were validated using 525 individuals with an average assignment accuracy of 83%. Thus, these GT-seq panels are powerful tools for assessing population structure and quantifying the relative contributions of populations/stocks in mixed-stock fisheries across multiple regions. Interweaving genomic data derived from these tools with Traditional Ecological Knowledge will ensure the sustainable harvest of three culturally important salmonids in Indigenous communities, contributing to food security programmes and the economy in Northern Canada.
Foraging decisions shape the structure of food webs. Therefore, a behavioural shift in a single species can potentially modify resource-flow dynamics of entire ecosystems. To examine this, we conducted a field experiment to assess foraging niche dynamics of semi-arboreal brown anole lizards in the presence/absence of predatory ground-dwelling curly-tailed lizards in a replicated set of island ecosystems. One year after experimental translocation, brown anoles exposed to these predators had drastically increased perch height and reduced consumption of marine-derived food resources. This foraging niche shift altered marine-to-terrestrial resource-flow dynamics and persisted in the diets of the first-generation offspring. Furthermore, female lizards that displayed more risk-taking behaviours consumed more marine prey on islands with predators present. Our results show how predator-driven rapid behavioural shifts can alter food-web connectivity between oceanic and terrestrial ecosystems and underscore the importance of studying behaviour-mediated niche shifts to understand ecosystem functioning in rapidly changing environments.
Effective population size (Ne) is a particularly useful metric for conservation as it affects genetic drift, inbreeding and adaptive potential within populations. Current guidelines recommend a minimum Ne of 50 and 500 to avoid short-term inbreeding and to preserve long-term adaptive potential respectively. However, the extent to which wild populations reach these thresholds globally has not been investigated, nor has the relationship between Ne and human activities. Through a quantitative review, we generated a dataset with 4610 georeferenced Ne estimates from 3829 populations, extracted from 723 articles. These data show that certain taxonomic groups are less likely to meet 50/500 thresholds and are disproportionately impacted by human activities; plant, mammal and amphibian populations had a <54% probability of reaching N ̂ e = 50 and a <9% probability of reaching N ̂ e = 500. Populations listed as being of conservation concern according to the IUCN Red List had a smaller median N ̂ e than unlisted populations, and this was consistent across all taxonomic groups. N ̂ e was reduced in areas with a greater Global Human Footprint, especially for amphibians, birds and mammals, however relationships varied between taxa. We also highlight several considerations for future works, including the role that gene flow and subpopulation structure plays in the estimation of N ̂ e in wild populations, and the need for finer-scale taxonomic analyses. Our findings provide guidance for more specific thresholds based on Ne and help prioritise assessment of populations from taxa most at risk of failing to meet conservation thresholds.
The environment plays an important role in the movement of individuals and their associated genes among populations, which facilitates gene flow. Gene flow can help maintain the genetic diversity both within and between populations and counter the negative impact of genetic drift, which can decrease the fitness of individuals. Sympatric species can have different habitat preferences, and thus can exhibit different patterns of genetic variability and population structure. The specialist-generalist variation hypothesis (SGVH) predicts that specialists will have lower genetic diversity, lower effective population sizes (Ne), and less gene flow among populations. In this study, we used spatially explicit, individual-based comparative approaches to test SGVH predictions in two sympatric cottontail species and identify environmental variables that influence their gene flow. New England cottontail (Sylvilagus transitionalis) is the only native cottontail in the Northeast US, an early successional habitat specialist, and a species of conservation concern. Eastern cottontail (S. floridanus) is an invasive species in the Northeast US and a habitat generalist. We characterized each species’ genomic variation by developing double-digest Restriction-site Associated DNA sequence single nucleotide polymorphism markers, quantified their habitat with Geographic Information System environmental variables, and conducted our analyses at multiple scales. Surprisingly, both species had similar levels of genetic diversity and eastern cottontail’s Ne was only higher than New England cottontail in one of three subregions. At a regional level, the population clusters of New England cottontail were more distinct than eastern cottontail, but the subregional levels showed more geographic areas of restricted gene flow for eastern cottontail than New England cottontail. In general, the environmental variables had the predicted effect on each species’ gene flow. However, the most important environmental variable varied by subregion and species, which shows that location and species matter. Our results provide partial support for the SGVH and the identification of environmental variables that facilitate or impede gene flow can be used to help inform management decisions to conserve New England cottontail.
In the state of Florida, USA, lizards of the genus Anolis are well represented with at least nine established non-native species and a single native species, A. carolinensis. The most recently introduced species is A. allisoni, a close relative to both the native A. carolinensis and one of the introduced species (A. porcatus). Anolis allisoni is thought to have been present in two locations in Florida since at least 2013 based on photographic evidence. Here, we analyzed mitochondrial DNA (mtDNA) sequences from these three closely related Anolis species to infer the most likely region of origin in the native range and confirm the establishment of the recent invader in Tampa, Florida. We found a single haplotype belonging to A. allisoni, which was closely related to native sequences from east-central Cuba. The most likely geographic origin is a tourist destination in the province of Sancti Spiritus, suggesting the potential for human-mediated introduction of A. allisoni to Florida. Given the evidence of hybridization within the carolinensis subgroup, the presence and establishment of the phylogenetically related and ecomorphologically similar A. allisoni may create novel opportunities for interspecific genetic exchange.
Hybridization is among the evolutionary mechanisms most frequently hypothesized to drive the success of invasive species, in part because hybrids are common in invasive populations. One explanation for this pattern is that biological invasions coincide with a change in selection pressures that limit hybridization in the native range. To investigate this possibility, we studied the introduction of the brown anole (Anolis sagrei) in the southeastern United States. We find that native populations are highly genetically structured. In contrast, all invasive populations show evidence of hybridization among native-range lineages. Temporal sampling in the invasive range spanning 15 y showed that invasive genetic structure has stabilized, indicating that large-scale contemporary gene flow is limited among invasive populations and that hybrid ancestry is maintained. Additionally, our results are consistent with hybrid persistence in invasive populations resulting from changes in natural selection that occurred during invasion. Specifically, we identify a large-effect X chromosome locus associated with variation in limb length, a well-known adaptive trait in anoles, and show that this locus is often under selection in the native range, but rarely so in the invasive range. Moreover, we find that the effect size of alleles at this locus on limb length is much reduced in hybrids among divergent lineages, consistent with epistatic interactions. Thus, in the native range, epistasis manifested in hybrids can strengthen extrinsic postmating isolation. Together, our findings show how a change in natural selection can contribute to an increase in hybridization in invasive populations.
Androdioecy (the coexistence of males and hermaphrodites) is a rare mating system for which the evolutionary dynamics are poorly understood. Here, we investigate the cottony cushion scale, Icerya purchasi, one of only three reported cases of androdioecy in insects. In this species, female-like hermaphrodites have been shown to produce sperm and self-fertilize. However, males are ocassionally observed as well. In a large genetic analysis, we show for the first time that, although self-fertilization appears to be the primary mode of reproduction, rare outbreeding events do occur in natural populations, supporting the hypothesis that hermaphrodites mate with males and hence androdioecy is the mating system of I. purchasi. Thus, this globally invasive pest insect appears to enjoy the colonization advantages of a selfing organism while also benefitting from periodic reintroduction of genetic variation through outbreeding with males.
Abstract As the rate of urbanization continues to increase globally, a growing body of research is emerging that investigates how urbanization shapes the movement—and consequent gene flow—of species in cities. Of particular interest are native species that persist in cities, either as small relict populations or as larger populations of synanthropic species that thrive alongside humans in new urban environments. In this study, we used genomic sequence data (SNPs) and spatially explicit individual‐based analyses to directly compare the genetic structure and patterns of gene flow in two small mammals with different dispersal abilities that occupy the same urbanized landscape to evaluate how mobility impacts genetic connectivity. We collected 215 white‐footed mice (Peromyscus leucopus) and 380 big brown bats (Eptesicus fuscus) across an urban‐to‐rural gradient within the Providence, Rhode Island (U.S.A.) metropolitan area (population =1,600,000 people). We found that mice and bats exhibit clear differences in their spatial genetic structure that are consistent with their dispersal abilities, with urbanization having a stronger effect on Peromyscus mice. There were sharp breaks in the genetic structure of mice within the Providence urban core, as well as reduced rates of migration and an increase in inbreeding with more urbanization. In contrast, bats showed very weak genetic structuring across the entire study area, suggesting a near‐panmictic gene pool likely due to the ability to disperse by flight. Genetic diversity remained stable for both species across the study region. Mice also exhibited a stronger reduction in gene flow between island and mainland populations than bats. This study represents one of the first to directly compare multiple species within the same urban‐to‐rural landscape gradient, an important gap to fill for urban ecology and evolution. Moreover, here we document the impacts of dispersal capacity on connectivity for native species that have persisted as the urban landscape matrix expands.
Human activities have reshaped patterns of island biogeography for many groups of amphibians and reptiles. In Trinidad, an island in the West Indies with only one native Anolis lizard species, four additional anole species have been introduced since the 1800s. The most recent introduction, Anolis wattsi, native to Antigua, has become established despite the presence of multiple species of resident anoles. We used genetic data (mitochondrial DNA) to infer the geographic origin and genetic structure of introduced A. wattsi on Trinidad. We then gathered published data to compare eco-morphological traits of all anole species currently established on the island. We found three mtDNA haplotypes in Trinidad that clustered with two different clades from the northern part of the native range in Antigua, rejecting the hypothesis that the lizards originated in the pineapple-growing region of the south. However, a lack of fine-scale population structure precluded precise identification of the origin in Antigua of haplotypes introduced to Trinidad. Compared to the other anole species on Trinidad, A. wattsi is smaller, perches lower, and has a higher field body temperature. Thus, the successful establishment and spread of A. wattsi should not be surprising given the success of two previous introductions of anole species that were more similar ecomorphologically to the native species and each other, and the fact that Trinidad has relatively few anole species for its size.
Small-bodied vertebrates sometimes evolve gigantism on islands, but there is a lack of consistent association with ecological factors or island characteristics. One possible reason is that, even if the ecological conditions are right, body size might fail to diverge on islands that were isolated recently or if there is gene flow between islands and the mainland. We studied body size, ventral colour polymorphism and genetic structure across nine islands and adjacent mainland populations of common wall lizards (Podarcis muralis) off the western coast of France. Population genetic data suggested that island populations might have maintained gene flow after their geographical isolation from the mainland. Island lizards were larger and heavier than mainland lizards on average, but the extent of gigantism varied substantially between islands. Island size and distance from the mainland were poor predictors of body size, but lizards from populations that were highly genetically differentiated from the mainland were larger than lizards from less differentiated populations. Colour morphs that were rare on the mainland tended to be more common on islands. We propose that genetic isolation or bottlenecks promote body size evolution in island lizards, which makes it challenging to identify ecological causes of island gigantism without complementary genetic information.
Urbanization is accelerating worldwide and creates novel habitat conditions including increases in environmental temperature and changes in presence and abundance of predators, prey and parasites. For species that use urban habitats, these changes can have strong impacts on phenotypes. Anolis lizards commonly exploit urban habitats and, as ectotherms, are likely to experience pressures from these novel environments. Previous research shows that anoles may adapt to some aspects of urban habitats, but we lack an understanding of the breadth of traits that may shift in response to urbanization and how widespread these changes may be. To assess effects of urban habitat use on anole phenotypes, we measured morphology, thermal preference and parasitism in brown anoles (Anolis sagrei) and crested anoles (Anolis cristatellus) from urban and natural habitats within the Miami metropolitan area (FL, USA). In urban areas, individuals of both species were larger, but did not show any differences in preferred body temperatures. These results agree with other studies showing increased body size in anoles inhabiting urban areas, but the mechanisms underlying this pattern are unclear. Brown anoles experienced higher levels of parasite infection intensity in urban habitats, but crested anoles showed no differences between urban and natural sites. Increased infection intensity in urban brown anoles suggests that exploiting urban habitats may have costs and shows that urbanization can lead to species-specific changes in ecologically similar congeners. Understanding how urban habitats alter phenotypes of organisms that exploit these areas will be important in predicting costs of and adaptive responses to future urbanization.
AimNatural range expansions and human-mediated colonizations usually involve a small number of individuals that establish new populations in novel habitats. In both cases, founders carry only a fraction of the total genetic variation of the source populations. Here, we used native and non-native populations of the green anole, Anolis carolinensis, to compare the current distribution of genetic variation in populations shaped by natural range expansion and human-mediated colonization. LocationNorth America, Hawaiian Islands, Western Pacific Islands. MethodsWe analysed 401 mtDNA haplotypes to infer the colonization history of A. carolinensis on nine islands in the Pacific Ocean. We then genotyped 576 individuals at seven microsatellite loci to assess the levels of genetic diversity and population genetic differentiation for both the native and non-native ranges. ResultsOur findings support two separate introductions to the Hawaiian Islands and several western Pacific islands, with subsequent colonizations within each region following a stepping-stone model. Genetic diversity at neutral markers was significantly lower in the non-native range because of founder effects, which also contributed to the increased population genetic differentiation among the non-native regions. In contrast, a steady reduction in genetic diversity with increasing distance from the ancestral population was observed in the native range following range expansion. Main conclusionsRange expansions cause serial founder events that are the spatial analogue of genetic drift, producing a pattern of isolation-by-distance in the native range of the species. In human-mediated colonizations, after an initial loss of genetic diversity, founder effects appear to persist, resulting in overall high genetic differentiation among non-native regions but an absence of isolation-by-distance. Contrasting the processes influencing the amount and structuring of genetic variability during natural range expansion and human-mediated biological invasions can shed new light on the fate of natural populations exposed to novel and changing environments.
Many populations are small and isolated with limited genetic variation and high risk of mating with close relatives. Inbreeding depression is suspected to contribute to extinction of wild populations, but the historical and demographic factors that contribute to reduced population viability are often difficult to tease apart. Replicated introduction events in non-native species can offer insights into this problem because they allow us to study how genetic variation and inbreeding depression are affected by demographic events (e.g. bottlenecks), genetic admixture and the extent and duration of isolation. Using detailed knowledge about the introduction history of 21 non-native populations of the wall lizard Podarcis muralis in England, we show greater loss of genetic diversity (estimated from microsatellite loci) in older populations and in populations from native regions of high diversity. Loss of genetic diversity was accompanied by higher embryonic mortality in non-native populations, suggesting that introduced populations are sufficiently inbred to jeopardize long-term viability. However, there was no statistical correlation between population-level genetic diversity and average embryonic mortality. Similarly, at the individual level, there was no correlation between female heterozygosity and clutch size, infertility or hatching success, or between embryo heterozygosity and mortality. We discuss these results in the context of human-mediated introductions and how the history of introductions can play a fundamental role in influencing individual and population fitness in non-native species.
Summary Divergence in sexually selected traits in allopatry should affect the degree and direction of hybridization. However, few studies have established the causes and targets of sexual selection during secondary contact. Common wall lizards (Podarcis muralis) from north‐central Italy have highly exaggerated male sexual traits compared to populations in Western Europe. Using experimental populations, we show that this creates asymmetries in male dominance, spatial habitat use and reproductive success upon secondary contact. Hybridization occurred almost exclusively between males of the Italian lineage and females of the Western European lineage. We provide evidence to suggest stronger ongoing selection on male sexual traits within the dominant Italian lineage. However, these same characters did not predict hybridization, and hybrid matings contributed little to variance in male reproductive success. Instead, most hybrid offspring were sired by Italian males displaying phenotypes associated with lower within‐lineage reproductive success. Thus, highly directional hybridization arises because some Italian males are out‐competed within their own lineage but remain competitive relative to males of the other lineage. This pattern of hybridization is consistent with the direction of introgression in natural contact zones, but our data suggest that sexual selection acting through hybridization may be weak at the leading edge of natural hybrid zones. A lay summary is available for this article.