From nature to the laboratory: the impact of founder effects on adaptation

Most founding events entail a reduction in population size, which in turn leads to genetic drift effects that can deplete alleles. Besides reducing neutral genetic variability, founder effects can in principle shift additive genetic variance for phenotypes that underlie fitness. This could then lead to different rates of adaptation among populations that have undergone a population size bottleneck as well as an environmental change, even when these populations have a common evolutionary history. Thus, theory suggests that there should be an association between observable genetic variability for both neutral markers and phenotypes related to fitness. Here, we test this scenario by monitoring the early evolutionary dynamics of six laboratory foundations derived from founders taken from the same source natural population of Drosophila subobscura. Each foundation was in turn three‐fold replicated. During their first few generations, these six foundations showed an abrupt increase in their genetic differentiation, within and between foundations. The eighteen populations that were monitored also differed in their patterns of phenotypic adaptation according to their immediately ancestral founding sample. Differences in early genetic variability and in effective population size were found to predict differences in the rate of adaptation during the first 21 generations of laboratory evolution. We show that evolution in a novel environment is strongly contingent not only on the initial composition of a newly founded population but also on the stochastic changes that occur during the first generations of colonization. Such effects make laboratory populations poor guides to the evolutionary genetic properties of their ancestral wild populations.     

Role of propagule pressure in colonization success: disentangling the relative importance of demographic,genetic and habitat effects

High propagule pressure is arguably the only consistent predictor of colonization success. More individuals enhance colonization success because they aid in overcoming demographic consequences of small population size (e.g. stochasticity and Allee effects). The number of founders can also have direct genetic effects: with fewer individuals, more inbreeding and thus inbreeding depression will occur, whereas more individuals typically harbour greater genetic variation. Thus, the demographic and genetic components of propagule pressure are interrelated, making it difficult to understand which mechanisms are most important in determining colonization success. We experimentally disentangled the demographic and genetic components of propagule pressure by manipulating the number of founders (fewer or more), and genetic background (inbred or outbred) of individuals released in a series of three complementary experiments. We used Bemisia whiteflies and released them onto either their natal host (benign) or a novel host (challenging). Our experiments revealed that having more founding individuals and those individuals being outbred both increased the number of adults produced, but that only genetic background consistently shaped net reproductive rate of experimental populations. Environment was also important and interacted with propagule size to determine the number of adults produced. Quality of the environment interacted also with genetic background to determine establishment success, with a more pronounced effect of inbreeding depression in harsh environments. This interaction did not hold for the net reproductive rate. These data show that the positive effect of propagule pressure on founding success can be driven as much by underlying genetic processes as by demographics. Genetic effects can be immediate and have sizable effects on fitness.     

Expansion history and environmental suitability shape effective population size in a plant invasion

The margins of an expanding range are predicted to be challenging environments for adaptation. Marginal populations should often experience low effective population sizes (N_e) where genetic drift is high due to demographic expansion and/or census population size is low due to unfavourable environmental conditions. Nevertheless, invasive species demonstrate increasing evidence of rapid evolution and potential adaptation to novel environments encountered during colonization, calling into question whether significant reductions in N_e are realized during range expansions in nature. Here we report one of the first empirical tests of the joint effects of expansion dynamics and environment on effective population size variation during invasive range expansion. We estimate contemporary values of N_e using rates of linkage disequilibrium among genome‐wide markers within introduced populations of the highly invasive plant Centaurea solstitialis (yellow starthistle) in North America (California, USA), and within native Eurasian populations. As predicted, we find that N_e within the invaded range is positively correlated with both expansion history (time since founding) and habitat quality (abiotic climate). History and climate had independent additive effects with similar effect sizes, indicating an important role for both factors in this invasion. These results support theoretical expectations for the population genetics of range expansion, though whether these processes can ultimately arrest the spread of an invasive species remains an unanswered question.     

Experimental island invasion of house mice

The ability of invasive species to recurrently establish populations from small numbers of founders, while threatened species struggle at the same low population sizes, is a paradox in conservation biology. Little is known about the mechanisms contributing to the post-arrival success of low density invasive populations as most invasive species research focuses on established, high density populations. Experimental studies are powerful, but generally limited to laboratory or invertebrate experiments. Here, we experimentally demonstrate that vertebrate mammal invasion from a very small (n = 2) number of founders follows relatively simple deterministic predictions. An intentional island invasion of introduced house mice (Mus musculus Linnaeus) from one founding pair closely tracked the density dependent logistic growth curve and reached the seasonal carrying capacity of a previously extant population in only 5 months. Carrying capacity reflected both density dependent and independent processes. In contrast to the previously incumbent population, the invading population retained a marked genetic signal of its recent founder event, but the populations were otherwise demographically indistinguishable. Stochastic events such as individual variability, supplemental immigration and ecological release, but not Allee effects, played important roles during colonisation, but following establishment dynamics rapidly became deterministic, with little demographic impact of reduced genetic diversity. The small population paradigm appears to have little influence on the population dynamics of highly successful invasive species.     

Effects of founding genetic variation on adaptation to a novel resource

Population genetic theory predicts that adaptation in novel environments is enhanced by genetic variation for fitness. However, theory also predicts that under strong selection, demographic stochasticity can drive populations to extinction before they can adapt. We exposed wheat-adapted populations of the flour beetle (Tribolium castaneum) to a novel suboptimal corn resource, to test the effects of founding genetic variation on population decline and subsequent extinction or adaptation. As previously reported, genetically diverse populations were less likely to go extinct. Here, we show that among surviving populations, genetically diverse groups recovered faster after the initial population decline. Within two years, surviving populations significantly increased their fitness on corn via increased fecundity, increased egg survival, faster larval development, and higher rate of egg cannibalism. However, founding genetic variation only enhanced the increase in fecundity, despite existing genetic variation-and apparent lack of trade-offs-for egg survival and larval development time. Thus, during adaptation to novel habitats the positive impact of genetic variation may be restricted to only a few traits, although change in many life-history traits may be necessary to avoid extinction. Despite severe initial maladaptation and low population size, genetic diversity can thus overcome the predicted high extinction risk in new habitats.     

The roles of demography and genetics in the early stages of colonization

Colonization success increases with the size of the founding group. Both demographic and genetic factors underlie this relationship, yet because genetic diversity normally increases with numbers of individuals, their relative importance remains unclear. Furthermore, their influence may depend on the environment and may change as colonization progresses from establishment through population growth and then dispersal. We tested the roles of genetics, demography and environment in the founding of Tribolium castaneum populations. Using three genetic backgrounds (inbred to outbred), we released individuals of four founding sizes (2–32) into two environments (natal and novel), and measured establishment success, initial population growth and dispersal. Establishment increased with founding size, whereas population growth was shaped by founding size, genetic background and environment. Population growth was depressed by inbreeding at small founding sizes, but growth rates were similar across genetic backgrounds at large founding size, an interaction indicating that the magnitude of the genetic effects depends upon founding population size. Dispersal rates increased with genetic diversity. These results suggest that numbers of individuals may drive initial establishment, but that subsequent population growth and spread, even in the first generation of colonization, can be driven by genetic processes, including both reduced growth owing to inbreeding depression, and increased dispersal with increased genetic diversity.     

Effects of multiple founder populations on spatial genetic structure of reintroduced American martens

Reintroductions and translocations are increasingly used to repatriate or increase probabilities of persistence for animal and plant species. Genetic and demographic characteristics of founding individuals and suitability of habitat at release sites are commonly believed to affect the success of these conservation programs. Genetic divergence among multiple source populations of American martens (Martes americana) and well documented introduction histories permitted analyses of post‐introduction dispersion from release sites and development of genetic clusters in the Upper Peninsula (UP) of Michigan <50 years following release. Location and size of spatial genetic clusters and measures of individual‐based autocorrelation were inferred using 11 microsatellite loci. We identified three genetic clusters in geographic proximity to original release locations. Estimated distances of effective gene flow based on spatial autocorrelation varied greatly among genetic clusters (30–90 km). Spatial contiguity of genetic clusters has been largely maintained with evidence for admixture primarily in localized regions, suggesting recent contact or locally retarded rates of gene flow. Data provide guidance for future studies of the effects of permeabilities of different land‐cover and land‐use features to dispersal and of other biotic and environmental factors that may contribute to the colonization process and development of spatial genetic associations.     

Long‐term ‘islands’ in the landscape: low gene flow,effective population size and genetic divergence in the shrub Hakea oldfieldii (Proteaceae)

The genetic structure of disjunct populations is determined by founding genetic properties, demographic processes, gene flow, drift and local selection. We aim to identify the genetic consequences of natural population disjunction at regional and local scales in Hakea oldfieldii using nuclear and plastid markers to investigate long‐term effective population sizes and gene flow, and patterns of diversity and divergence, among populations. Regional divergence was significant as shown by a consistent pattern in principal coordinates, neighbor‐joining and Bayesian analyses, but divergence at the local level was also significant with localized distribution of plastid haplotypes and populations clustering separately in Bayesian analyses. Historical, recent and first‐generation gene flow was low, suggesting that recent habitat fragmentation has not reduced gene migration significantly. Genetic bottlenecks were detected in three populations. Long‐term effective population size was significantly correlated with the number of alleles/locus and observed heterozygosity, but not with census population size, suggesting that the loss of diversity is associated with long‐term changes rather than recent fragmentation. Inbreeding coefficients were significant in only three populations, suggesting that the loss of diversity is linked to drift and bottlenecks associated with demographic processes (local extinction by fires) rather than inbreeding. Historical disjunction as a result of specific ecological requirements, contraction of habitats following drying during the Pleistocene, low gene flow and changes in population size are likely to have been important forces driving divergence through isolation by distance and drift. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 319–334.     

Fast evolutionary genetic differentiation during experimental colonizations

Founder effects during colonization of a novel environment are expected to change the genetic composition of populations, leading to differentiation between the colonizer population and its source population. Another expected outcome is differentiation among populations derived from repeated independent colonizations starting from the same source. We have previously detected significant founder effects affecting rate of laboratory adaptation among Drosophila subobscura laboratory populations derived from the wild. We also showed that during the first generations in the laboratory, considerable genetic differentiation occurs between foundations. The present study deepens that analysis, taking into account the natural sampling hierarchy of six foundations, derived from different locations, different years and from two samples in one of the years. We show that striking stochastic effects occur in the first two generations of laboratory culture, effects that produce immediate differentiation between foundations, independent of the source of origin and despite similarity among all founders. This divergence is probably due to powerful genetic sampling effects during the first few generations of culture in the novel laboratory environment, as a result of a significant drop in N _e. Changes in demography as well as high variance in reproductive success in the novel environment may contribute to the low values of N _e. This study shows that estimates of genetic differentiation between natural populations may be accurate when based on the initial samples collected in the wild, though considerable genetic differentiation may occur in the very first generations of evolution in a new, confined environment. Rapid and significant evolutionary changes can thus occur during the early generations of a founding event, both in the wild and under domestication, effects of interest for both scientific and conservation purposes.     

Conservation of population structure and genetic diversity under captive breeding of remnant coaster brook trout (<Emphasis Type="Italic">Salvelinus fontinalis</Emphasis>) populations

Rebuilding wild populations often involves captive broodstocks derived from small, remnant populations. We measured a hatchery program’s ability to conserve genetic diversity when founding captive broodstocks from such populations. Migratory coaster brook trout were extirpated from most of their historic range in US waters of Lake Superior and were proposed for listing under the Endangered Species Act. Two captive broodstocks, one with 19 founders and another with 99 founders, were established to rebuild US populations. We used microsatellite markers to examine genetic variation in source populations and early hatchery generations. Broodstocks retained the strong differentiation found between source populations; however, one founder, with a low probability of belonging to either source population, sired 5.7% of F₁ progeny. We found small changes in within-population genetic variation across successive wild and hatchery generations of broodstocks. Evaluation of stage-specific survivorship indicated that equalizing family sizes of embryos produced modest gains in the effective number of breeders, and that survival in the hatchery was nearly random across families. Our study demonstrates the value of genetic monitoring during initial stages of hatchery programs for small and declining populations.     

Demographic factors and genetic variation influence population persistence under environmental change

Population persistence has been studied in a conservation context to predict the fate of small or declining populations. Persistence models have explored effects on extinction of random demographic and environmental fluctuations, but in the face of directional environmental change they should also integrate factors affecting whether a population can adapt. Here, we examine the population‐size dependence of demographic and genetic factors and their likely contributions to extinction time under scenarios of environmental change. Parameter estimates were derived from experimental populations of the rainforest species, Drosophila birchii, held in the lab for 10 generations at census sizes of 20, 100 and 1000, and later exposed to five generations of heat‐knockdown selection. Under a model of directional change in the thermal environment, rapid extinction of populations of size 20 was caused by a combination of low growth rate (r) and high stochasticity in r. Populations of 100 had significantly higher reproductive output, lower stochasticity in r and more additive genetic variance (V_A) than populations of 20, but they were predicted to persist less well than the largest size class. Even populations of 1000 persisted only a few hundred generations under realistic estimates of environmental change because of low V_A for heat‐knockdown resistance. The experimental results document population‐size dependence of demographic and adaptability factors. The simulations illustrate a threshold influence of demographic factors on population persistence, while genetic variance has a more elastic impact on persistence under environmental change.     

Optimizing the genetic composition of a translocation population: Incorporating constraints and conflicting objectives

Translocations of threatened species can reduce the risk of extinction from a catastrophic event. For plants, translocation consists of moving individuals, seeds, or cuttings from a native (source) population to a new site. Ideally a translocation population would be genetically diverse and consist of fit founding individuals. In practice, there are challenges to designing such a population, including constraints on the availability of material, and tradeoffs between different goals. Here, we present an approach for designing a translocation population that identifies sets of founders that are optimized according to multiple criteria (e.g., genetic diversity), while also conforming to constraints on the representation of different founders (e.g., propagation success). It uses flexible inputs, including SNP genotypes, matrices of similarity between individuals, and vectors of phenotype data. We apply the approach to a critically endangered plant, Hibbertia puberula subsp. glabrescens (Dilleniaceae), which was genotyped at thousands of SNP loci. The goals of minimizing genetic similarity among the founding individuals and maximizing genetic diversity were largely complementary: populations optimized for one of these criteria were near‐optimal for the other. We also performed analyses in which we minimized genetic similarity among founding individuals while imposing selection (against hypothetical deleterious alleles, and against undesirable phenotypes, respectively), and here characterized sharp tradeoffs. This was useful in allowing the benefits of selection to be weighed against costs in terms of genetic similarity. In summary, we present an approach for designing a translocation population that allows flexible inputs, the imposition of realistic constraints, and examination of conflicting goals.     

Insights into the neutral and adaptive processes shaping the spatial distribution of genomic variation in the economically important Moroccan locust (Dociostaurus maroccanus)

Understanding the processes that shape neutral and adaptive genomic variation is a fundamental step to determine the demographic and evolutionary dynamics of pest species. Here, we use genomic data obtained via restriction site‐associated DNA sequencing to investigate the genetic structure of Moroccan locust (Dociostaurus maroccanus) populations from the westernmost portion of the species distribution (Iberian Peninsula and Canary Islands), infer demographic trends, and determine the role of neutral versus selective processes in shaping spatial patterns of genomic variation in this pest species of great economic importance. Our analyses showed that Iberian populations are characterized by high gene flow, whereas the highly isolated Canarian populations have experienced strong genetic drift and loss of genetic diversity. Historical demographic reconstructions revealed that all populations have passed through a substantial genetic bottleneck around the last glacial maximum (~21 ka BP) followed by a sharp demographic expansion at the onset of the Holocene, indicating increased effective population sizes during warm periods as expected from the thermophilic nature of the species. Genome scans and environmental association analyses identified several loci putatively under selection, suggesting that local adaptation processes in certain populations might not be impeded by widespread gene flow. Finally, all analyses showed few differences between outbreak and nonoutbreak populations. Integrated pest management practices should consider high population connectivity and the potential importance of local adaptation processes on population persistence.     

INCREASED PROBABILITY OF EXTINCTION DUE TO DECREASED GENETIC EFFECTIVE POPULATION SIZE: EXPERIMENTAL POPULATIONS OF CLARKIA PULCHELLA

We established replicated experimental populations of the annual plant Clarkia pulchella to evaluate the existence of a causal relationship between loss of genetic variation and population survival probability. Two treatments differing in the relatedness of the founders, and thus in the genetic effective population size (N_e), were maintained as isolated populations in a natural environment. After three generations, the low N_e treatment had significantly lower germination and survival rates than did the high N_e treatment. These lower germination and survival rates led to decreased mean fitness in the low N_e populations: estimated mean fitness in the low N_e populations was only 21% of the estimated mean fitness in the high N_e populations. This inbreeding depression led to a reduction in population survival: at the conclusion of the experiment, 75% of the high N_e populations were still extant, whereas only 31% of the low N_e populations had survived. Decreased genetic effective population size, which leads to both inbreeding and the loss of alleles by genetic drift, increased the probability of population extinction over that expected from demographic and environmental stochasticity alone. This demonstrates that the genetic effective population size can strongly affect the probability of population persistence.     

Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions

Invasive species are predicted to suffer from reductions in genetic diversity during founding events, reducing adaptive potential. Integrating evidence from two literature reviews and two case studies, we address the following questions: How much genetic diversity is lost in invasions? Do multiple introductions ameliorate this loss? Is there evidence for loss of diversity in quantitative traits? Do invaders that have experienced strong bottlenecks show adaptive evolution? How do multiple introductions influence adaptation on a landscape scale? We reviewed studies of 80 species of animals, plants, and fungi that quantified nuclear molecular diversity within introduced and source populations. Overall, there were significant losses of both allelic richness and heterozygosity in introduced populations, and large gains in diversity were rare. Evidence for multiple introductions was associated with increased diversity, and allelic variation appeared to increase over long timescales (~100 years), suggesting a role for gene flow in augmenting diversity over the long‐term. We then reviewed the literature on quantitative trait diversity and found that broad‐sense variation rarely declines in introductions, but direct comparisons of additive variance were lacking. Our studies of Hypericum canariense invasions illustrate how populations with diminished diversity may still evolve rapidly. Given the prevalence of genetic bottlenecks in successful invading populations and the potential for adaptive evolution in quantitative traits, we suggest that the disadvantages associated with founding events may have been overstated. However, our work on the successful invader Verbascum thapsus illustrates how multiple introductions may take time to commingle, instead persisting as a ‘mosaic of maladaptation’ where traits are not distributed in a pattern consistent with adaptation. We conclude that management limiting gene flow among introduced populations may reduce adaptive potential but is unlikely to prevent expansion or the evolution of novel invasive behaviour.     

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.     

Origin and patterns of genetic diversity of German fallow deer as inferred from mitochondrial DNA

Although not native to Germany, fallow deer (Dama dama) are commonly found today, but their origin as well as the genetic structure of the founding members is still unclear. In order to address these aspects, we sequenced ~400 bp of the mitochondrial d-loop of 365 animals from 22 locations in nine German Federal States. Nine new haplotypes were detected and archived in GenBank. Our data produced evidence for a Turkish origin of the German founders. However, German fallow deer populations have complex patterns of mtDNA variation. In particular, three distinct clusters were identified: Schleswig-Holstein, Brandenburg/Hesse/Rhineland and Saxony/lower Saxony/Mecklenburg/Westphalia/Anhalt. Signatures of recent demographic expansions were found for the latter two. An overall pattern of reduced genetic variation was therefore accompanied by a relatively strong genetic structure, as highlighted by an overall Phict value of 0.74 (P < 0.001).     

Modelling the effects of genetics and habitat on the demography of a grassland herb

There is growing evidence that genetic and ecological factors interact in determining population persistence. The demographic effects of inbreeding depression can largely depend on the ecological milieu. We used demographic data of the perennial herb Succisa pratensis from six populations in grazed and ungrazed sites with different soil moisture. We built an individual-based model assessing the demographic consequences of inbreeding depression in populations with different management and habitat. Today this plant has to cope with severe landscape fragmentation, deteriorating habitat conditions in terms of decreasing grazing intensity, and the effects of inbreeding depression. For each population we performed simulations testing two inbreeding depression hypotheses (partial dominance and overdominance) and three epistatic functions among loci. The results indicated stronger inbreeding depression effects for populations in unfavourable sites without grazing or in xeric habitats compared to populations in favourable mesic sites with grazing. Overall, we found stronger effects with overdominance, a result that emphasizes the importance of understanding the genetic mechanisms of inbreeding depression. Hence, management practices can interact with the genetic consequences of inbreeding depression in population dynamics, which may have important implications for plant population ecology and evolutionary dynamics of inbreeding depression.     

Demographic fluctuations lead to rapid and cyclic shifts in genetic structure among populations of an alpine butterfly,Parnassius smintheus

Many populations, especially in insects, fluctuate in size, and periods of particularly low population size can have strong effects on genetic variation. Effects of demographic bottlenecks on genetic diversity of single populations are widely documented. Effects of bottlenecks on genetic structure among multiple interconnected populations are less studied, as are genetic changes across multiple cycles of demographic collapse and recovery. We take advantage of a long‐term data set comprising demographic, genetic and movement data from a network of populations of the butterfly, Parnassius smintheus, to examine the effects of fluctuating population size on spatial genetic structure. We build on a previous study that documented increased genetic differentiation and loss of spatial genetic patterns (isolation by distance and by intervening forest cover) after a network‐wide bottleneck event. Here, we show that genetic differentiation was reduced again and spatial patterns returned to the system extremely rapidly, within three years (i.e. generations). We also show that a second bottleneck had similar effects to the first, increasing differentiation and erasing spatial patterns. Thus, bottlenecks consistently drive random divergence of allele frequencies among populations in this system, but these effects are rapidly countered by gene flow during demographic recovery. Our results reveal a system in which the relative influence of genetic drift and gene flow continually shift as populations fluctuate in size, leading to cyclic changes in genetic structure. Our results also suggest caution in the interpretation of patterns of spatial genetic structure, and its association with landscape variables, when measured at only a single point in time.     

Using genetic data to advance stream fish reintroduction science: a case study in brook trout

Widespread extirpation of native fish populations has led to a rise in species reintroduction efforts worldwide. Most efforts have relied on demographic data alone to guide project design and evaluate success. However, the genetic characteristics of many imperiled fish populations including low diversity, local adaptation, and hatchery introgression emphasize the importance of genetic data in the design and monitoring of reintroduction efforts. Focusing on a case study of brook trout (Salvelinus fontinalis) in North Carolina, we show how the combined use of genetic and demographic data can support reintroduction efforts by improving source population selection and providing opportunities to evaluate genetic viability and adaptive potential in restored populations. Using this combined approach, we reintroduced brook trout into a restored stream from two source populations and monitored changes in genetic diversity and population size in source and recipient populations. Three years after the initial translocation, the reintroduced population had comparable density, but higher genetic diversity, than either source population. This study demonstrates the utility of genetic and demographic data for reintroduction efforts, particularly when extant populations are genetically depauperate and maintaining adaptive potential is a primary restoration goal. However, we emphasize the value of continued monitoring at longer temporal and spatial scales to determine the effects of stochastic process on the long-term adaptive capacity and persistence of reintroduced populations. Overall, inclusion of genetic data in reintroduction efforts offers increased ability to meet project goals while simultaneously conserving critical sources of adaptive variation that exist across the landscape.