Founder events as determinants of within-island and among-island genetic structure of Daphnia metapopulations

The genetic structure of metapopulations offers insights into the genetic consequences of local extinction and recolonization. We studied allozyme variation in rock pool metapopulations of two species of waterfleas (Daphnia) with the aim to understand how these dynamics influence genetic differentiation. We screened 138 populations of D. magna and 65 populations of D. longispina from an area in the archipelago of southern Finland. The pools from which they were sampled are separated by distances between 1.5 and 4710 m and located on a total of 38 islands. The genetic population structure of the two species was strikingly similar, consistent with their similar metapopulation ecology. The mean F(PT) value (differentiation among pools with respect to the total metapopulation) was 0.55 and a hierarchical analysis showed that genetic differentiation was strong (>0.25) among pools within islands as well as among whole islands. Within islands, pairwise genetic differentiation increased with geographic distance, indicating isolation by distance due to spatially limited dispersal. Previous studies have shown strong founder events occurring during colonization in our metapopulation. We suggest that the genetic population structure in the studied metapopulations is largely explained by three consequences of these founder events: (i) strong drift during colonization, (ii) local inbreeding, which results in hybrid vigour and increased effective migration rates after subsequent immigration, and (iii) effects of selection through hitchhiking of neutral genes with linked loci under selection.     

Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers.

Population bottlenecks are often invoked to explain low levels of genetic variation in natural populations, yet few studies have documented the direct genetic consequences of known bottlenecks in the wild. Empirical studies of natural population bottlenecks are therefore needed, because key assumptions of theoretical and laboratory studies of bottlenecks may not hold in the wild. Here we present microsatellite data from a severe bottleneck (95% mortality) in an insular population of song sparrows (Melospiza melodia). The major findings of our study are as follows: (i) The bottleneck reduced heterozygosity and allelic diversity nearly to neutral expectations, despite non-random survival of birds with respect to inbreeding and wing length. (ii) All measures of genetic diversity regained pre-bottleneck levels within two to three years of the crash. This rapid recovery was due to low levels of immigration. (iii) The rapid recovery occurred despite a coincident, strong increase in average inbreeding. These results show that immigration at levels that are hard to measure in most field studies can lead to qualitatively very different genetic outcomes from those expected from mutations only. We suggest that future theoretical and empirical work on bottlenecks and metapopulations should address the impact of immigration.     

Genetic load,inbreeding depression and heterosis in an age‐structured metapopulation

In a metapopulation, the process of recurrent local extinction and recolonization gives rise to an age structure among demes. Recently established demes will tend to differ from older demes in terms of the levels of genetic diversity found within them and the way this diversity is distributed among demes in the same and different ages. The effects of population turnover on average levels of genetic diversity among demes in a metapopulation have been the focus of much attention, both for neutral and nonneutral loci, but much less is known about the distribution of nonneutral genetic diversity among demes of different ages. In this paper, we used computer simulations to study the distribution of genetic load, inbreeding depression and heterosis in an age‐structured metapopulation. We found that, for mildly deleterious mutations, within‐deme inbreeding depression increased, whereas heterosis and genetic load decreased with deme age following severe colonization bottlenecks. In contrast, recessive lethal alleles tended to be purged during colonization, with older populations showing higher genetic load and higher within‐deme inbreeding depression. Heterosis caused by recessive lethal alleles and resulting from gene flow among different demes tended to be greatest for young demes, because the mutations responsible tended to be purged in the first few generations after colonization, but its effects increased again as populations grow older as a result of immigration. Our results point to a need for estimates of genetic diversity, genetic load, within‐deme inbreeding depression and heterosis in demes of different age classes separately.     

Spatiotemporal structure of genetic variation of a spreading plant metapopulation on dynamic riverbanks along the Meuse River

Long-distance seed dispersal is a crucial determinant of within-population genetic variability and among-population genetic differentiation in plant metapopulations undergoing recurrent local extinctions and (re-)colonization. We investigated the spatial and temporal structure of genetic variation in a metapopulation of Sisymbrium austriacum located along a dynamic river system using dominant AFLP markers. Data on riverbank dynamics and colonization history allowed separating populations based on their age (< or =5 vs >5 years old). Bayesian analysis of population genetic structure indicated that populations were significantly differentiated from each other, but Mantel tests revealed that there was no relationship between pairwise geographic and genetic distances, suggesting that long-distance seed dispersal partly determines spatial genetic structure. Recent populations were less differentiated from each other than old populations. Analysis of molecular variance (AMOVA) indicated that both spatial factors and population age significantly determined genetic diversity, the effects of age being more important than spatial location. Clustering analysis revealed five large clusters, which were related primarily to population age and to a minor extent to geographical location. Our results indicate that the recurrent formation and destruction of riverbank habitats following peak flow events have a large impact on genetic diversity of riparian plant species.     

Bottlenecks drive temporal and spatial genetic changes in alpine caddisfly metapopulations

Background

Extinction and re-colonisation of local populations is common in ephemeral habitats such as temporary streams. In most cases, such population turnover leads to reduced genetic diversity within populations and increased genetic differentiation among populations due to stochastic founder events, genetic drift, and bottlenecks associated with re-colonisation. Here, we examined the spatio-temporal genetic structure of 8 alpine caddisfly populations inhabiting permanent and temporary streams from four valleys in two regions of the Swiss Alps in years before and after a major stream drying event, the European heat wave in summer 2003.

Results

We found that population turnover after 2003 led to a loss of allelic richness and gene diversity but not to significant changes in observed heterozygosity. Within all valleys, permanent and temporary streams in any given year were not differentiated, suggesting considerable gene flow and admixture between streams with differing hydroperiods. Large changes in allele frequencies after 2003 resulted in a substantial increase in genetic differentiation among valleys within one to two years (1-2 generations) driven primarily by drift and immigration. Signatures of genetic bottlenecks were detected in all 8 populations after 2003 using the M-ratio method, but in no populations when using a heterozygosity excess method, indicating differential sensitivity of bottleneck detection methods.

Conclusions

We conclude that genetic differentiation among A. uncatus populations changed markedly both temporally and spatially in response to the extreme climate event in 2003. Our results highlight the magnitude of temporal population genetic changes in response to extreme events. More specifically, our results show that extreme events can cause rapid genetic divergence in metapopulations. Further studies are needed to determine if recovery from this perturbation through gradual mixing of diverged populations by migration and gene flow leads to the pre-climate event state, or whether the observed changes represent a new genetic equilibrium.     

A century of genetic change and metapopulation dynamics in the Galápagos warbler finches (Certhidea)

Populations that are connected by immigrants play an important role in evolutionary and conservation biology, yet we have little direct evidence of how such metapopulations change genetically over evolutionary time. We compared historic (1894–1906) to modern (1988–2006) genetic variation in 11 populations of warbler finches at 14 microsatellite loci. Although several lines of evidence suggest that Darwin's finches may be in decline, we found that the genetic diversity of warbler finches has not generally declined, and broad‐scale patterns of variation remained similar over time. Contrary to expectations, inferred population sizes have generally increased over time (6–8%) as have immigration rates (8–16%), which may reflect a recent increase in the frequency and intensity of El Niño events. Individual island populations showed significant declines (18–19%) and also substantial gains (18–20%) in allelic richness over time. Changes in genetic diversity were correlated with changes in immigration rates, but did not correspond to population size or human disturbance. These results reflect the expected stabilizing properties of whole metapopulations over time. However, the dramatic and unpredictable changes observed in individual populations during this short time interval suggests that care should be taken when monitoring individual population fragments with snapshots of genetic variation.     

Colonization of vegetation-rich moraines and inference of multiple sources of colonization in the High Arctic for Salix arctica

Vegetation-rich patches in the High Arctic may serve as a significant source for vegetation reconstruction in the climate changes. Diversity and colonization, however, of such potential source populations in the High Arctic has rarely been studied. We examined chloroplast sequence variation in Salix arctica, a key species in the Canadian High Arctic, from four adjacent glacial moraines of differing ages on Ellesmere Island, Canada, as well as two other populations located at the center and southern end of the species’ range. The estimated ages of the moraines varied from 35,000 to 250 years old. The older moraine populations showed higher within-population genetic variation compared with the other moraine populations, which is generally attributed to differences in establishment age associated with plant densities among moraines. The moraines with smaller plant density had lower genetic diversity and had no private haplotypes, indicating the local population size and genetic diversity may not be recovered within a few thousand years. This suggests seed dispersal at a local scale may be limited even in species with high velocity of seed dispersal, and that High Arctic vegetation-rich patches may serve as significant source populations for sustaining local genetic diversity. In addition, the three regions we observed comprised an evolutionarily distinct lineage and significant population differentiation. This implies multiple sources for the colonization during the most recent deglaciation, resulting in the current wide distribution. Local as well as range-wide processes of colonization would be essential to understand vegetation responses in High Arctic to the environmental changes.     

Genetic structure of kestrel populations and colonization of the Cape Verde archipelago

Genetic diversity and population structure were studied in eight populations of the kestrel Falco tinnunculus to identify the genetic consequences of spatial distribution and to infer the colonization patterns of the Cape Verde archipelago. We studied genetic differentiation and gene flow among seven island populations and one mainland population using nine microsatellite loci. Within the archipelago, differentiation was strong and genetic diversity and heterozygosity were low but variable among populations. Two subspecies F. tinnunculus neglectus on the northwestern islands and F. tinnunculus alexandri on all the other islands were identified as genetically distinct units. F. t. alexandri could be further separated into two groups on eastern and southern islands. Populations are probably founded by birds originating from the mainland. Immigration is more likely to the eastern and southern populations, whereas the northwestern islands with the lowest genetic diversity and highest differentiation are likely to exhibit fewer founding events by immigrants. The number of founding events on each island may depend not only on geographical distance to neighbouring populations, but also on directional immigration due to the northeastern trade winds. This may explain differences in genetic differentiation and diversity between populations and subspecies and may enable allopatric speciation.     

Parasite‐mediated selection in a natural metapopulation of Daphnia magna

Parasite‐mediated selection varying across time and space in metapopulations is expected to result in host local adaptation and the maintenance of genetic diversity in disease‐related traits. However, nonadaptive processes like migration and extinction‐(re)colonization dynamics might interfere with adaptive evolution. Understanding how adaptive and nonadaptive processes interact to shape genetic variability in life‐history and disease‐related traits can provide important insights into their evolution in subdivided populations. Here we investigate signatures of spatially fluctuating, parasite‐mediated selection in a natural metapopulation of Daphnia magna. Host genotypes from infected and uninfected populations were genotyped at microsatellite markers, and phenotyped for life‐history and disease traits in common garden experiments. Combining phenotypic and genotypic data a Q_ST–F_ST‐like analysis was conducted to test for signatures of parasite mediated selection. We observed high variation within and among populations for phenotypic traits, but neither an indication of host local adaptation nor a cost of resistance. Infected populations have a higher gene diversity (Hs) than uninfected populations and Hs is strongly positively correlated with fitness. These results suggest a strong parasite effect on reducing population level inbreeding. We discuss how stochastic processes related to frequent extinction‐(re)colonization dynamics as well as host and parasite migration impede the evolution of resistance in the infected populations. We suggest that the genetic and phenotypic patterns of variation are a product of dynamic changes in the host gene pool caused by the interaction of colonization bottlenecks, inbreeding, immigration, hybrid vigor, rare host genotype advantage and parasitism. Our study highlights the effect of the parasite in ameliorating the negative fitness consequences caused by the high drift load in this metapopulation.     

Low genetic diversity and local adaptive divergence of Dracaena cambodiana (Liliaceae) populations associated with historical population bottlenecks and natural selection: an endangered long‐lived tree endemic to Hainan Island,China

Historical population bottlenecks and natural selection have important effects on the current genetic diversity and structure of long‐lived trees. Dracaena cambodiana is an endangered, long‐lived tree endemic to Hainan Island, China. Our field investigations showed that only 10 populations remain on Hainan Island and that almost all have been seriously isolated and grow in distinct habitats. A considerable amount of genetic variation at the species level, but little variation at the population level, and a high level of genetic differentiation among the populations with limited gene flow in D. cambodiana were detected using inter‐simple sequence repeat (ISSR) and random amplified polymorphic DNA (RAPD) analyses. No significant correlation was found between genetic diversity and actual population size, as the genetic diversities were similar regardless of population size. The Mantel test revealed that there was no correlation between genetic and geographic distances among the 10 populations. The UPGMA, PCoA and Bayesian analyses showed that local adaptive divergence has occurred among the D. cambodiana populations, which was further supported by habitat‐private fragments. We suggest that the current genetic diversity and population differentiation of D. cambodiana resulted from historical population bottlenecks and natural selection followed by historical isolation. However, the lack of natural regeneration of D. cambodiana indicates that former local adaptations with low genetic diversity may have been genetically weak and are unable to adapt to the current ecological environments.     

Highest genetic diversity at the northern range limit of the rare orchid Isotria medeoloides

Populations in previously glaciated regions are often genetically depauperate in comparison with populations at lower latitudes, due either to bottlenecks experienced in post-glacial colonization or to contemporary genetic drift in small, peripheral populations. Populations of the rare self-fertilizing North American orchid Isotria medeoloides are largest in the previously glaciated region near the northern range limit, allowing us to examine the role of historical versus contemporary processes in determining population genetic diversity and structure. If contemporary processes predominate, genetic diversity should increase with increasing census size. In contrast, if sequential bottlenecks associated with colonization are paramount, diversity should decrease with latitude and be relatively insensitive to census size. We genotyped 299 individuals from 20 populations at four variable microsatellite loci to contrast genetic diversity and structure for populations in previously glaciated regions versus previously unglaciated regions. Populations were highly inbred (F=0.95) and highly differentiated (R(ST)=0.485). Across all sampled populations, genetic diversity decreased and genetic differentiation increased with declining population size. Small southern populations were especially differentiated and genetically depauperate. In the glaciated part of the range, genetic diversity increased as populations approached the northern range limit, demonstrating the centrality of contemporary processes for this post-glacial colonist.     

Recovery process of genetic diversity through seed and pollen immigration at the northernmost leading-edge population of Fagus crenata

The range expansion of a plant species begins with colonization of ecological empty patches from posterior source populations. This process involves stochastic loss of genetic diversity. However, the founder population could restore genetic diversity by gene flow from posterior populations via seeds and pollen and its recovery affects evolutionary potential for species expansion. To clarify the recovery process of genetic diversity during species range expansion, gene flow via seeds and pollen was investigated at the expansion front of Fagus crenata. Based on eight nuclear microsatellite genotypes of a total of 150 individuals and 225 seeds at the northernmost leading-edge population, genetic diversity, fine-scale spatial genetic structure (FSGS), and genetic differentiation from other five northern populations were investigated. Moreover, both seed and pollen immigration and their effects on genetic diversity at different successional stages were analyzed. The leading-edge population showed lower genetic diversity and substantial genetic differentiation, reflecting its strong genetic drift. Non-significant FSGS and a negative inbreeding coefficient for mature trees may indicate that the earliest generation consisted of founders from foreign seed sources. The significant proportion of seed and pollen immigration increased the number of different alleles for later successional stages. The effective number of pollen parents from foreign sources (20.8) was markedly higher than that from the local source (2.1). These results indicated that pollen immigration incorporated new and rare alleles and increased the genetic diversity of the population. However, the proportion of foreign gene flow decreased during succession, probably due to the increased reproductive success of local individuals as they reached maturity and grew in size.     

Northwestern song sparrow populations show genetic effects of sequential colonization

Two genetic consequences are often considered evidence of a founder effect: substantial loss in genetic diversity and rapid divergence between source and founder populations. Single-step founder events have been studied for these effects, but with mixed results, causing continued controversy over the role of founder events in divergence. Experiments of serial bottlenecks have shown losses of diversity, increased divergence, and rapid behavioural changes possibly leading to reproductive isolation between source and final populations. The few studies conducted on natural, sequentially founded systems show some evidence of these effects. We examined a natural vertebrate system of sequential colonization among northwestern song sparrows (Melospiza melodia). This system has an effectively linear distribution, it was probably colonized within the last 10,000 years, there are morphological and behavioural differences among populations, and the westernmost populations occur in atypical habitats for the species. Eight microsatellite loci from eight populations in Alaska and British Columbia (n = 205) showed stepwise loss of genetic diversity, genetic evidence for strong population bottlenecks, and increased population divergence. The endpoint population on Attu Island has extremely low diversity (H(E) = 0.18). Our study shows that sequential bottlenecks or founder events can have powerful genetic effects in reducing diversity, possibly leading to rapid evolutionary divergence.     

大仓鼠年龄组及性别群体的遗传多样性

本文应用随机扩增多态性DNA (RAPD) 技术, 采用多态位点率、Shannon 信息多样性指数和Nei 遗传多样性指数作为种群遗传变异的指标, 研究了1998 和1999 年大仓鼠种群性别群体和年龄组群体的遗传多样性。主要的结论是: 性别群体间遗传分化较小, 年龄组群体间分化较大; 年龄组相距越大, 遗传分化也就越大; 幼年组的遗传多样性高于老龄组的遗传多样性; 1999 年秋季种群的年龄组遗传分化和差异要比1998 年四季种群更为明显。大仓鼠不同年龄组群体间的遗传分化支持遗传结构由于受时空上的选择压力而产生变异和适应性观点。大仓鼠幼体的遗传多样性比成体和老体的较高, 这一结果倾向于支持Ford 的假说, 说明种群繁殖出的幼体遗传多样性高, 其中有遗传质量好的, 也有遗传质量差的,但在生存过程中, 随着选择压力的作用, 种群趋于适应, 与环境不相适应的类型遭到淘汰,低质的幼体由于自然选择压力的增加而从种群中消失, 致使成年和老年群体多态性逐渐降低。     

Population biology of the invasive freshwater snail Physa acuta approached through genetic markers, ecological characterization and demography

Abstract The respective role of factors acting on population functioning can be inferred from a variety of approaches, including population genetics and demography. We here investigated the role of four of these factors (mating systems, population size, bottlenecks and migration) in the hermaphroditic freshwater snail Physa acuta. Twenty-four populations were sampled either around Montpellier (local scale), or at the scale of France (global scale). At local scale, eight populations were sampled twice, before and after summer drying out. The genetic structure of these populations was studied using microsatellite loci. Populations were classified according to openness (ponds vs. rivers) and water regime (permanent vs. temporary) allowing predictions on genetic patterns (e.g. diversity within populations and differentiation). At local scale, progeny-arrays analysis of the selfing rate was conducted, and size distributions of individuals were followed over two years. Results with regard to the four factors mentioned above were: (i) Estimates of population selfing rates derived from inbreeding coefficients were only slightly higher than those from progeny-arrays. (ii) More variation was detected in rivers than in ponds, but no influence of water regime was detected. One reason might be that permanent populations are not going less often through low densities than those from temporary habitats at the time scale studied. (iii) There was limited evidence for genetic bottlenecks which is compatible with the fact that even marked reduction in water availability was not necessarily associated with demographic bottlenecks. More generally, bottlenecks reducing genetic variation probably occur at population foundation. (iv) Lower genetic differentiation was detected among rivers than among ponds which might be related to limitations on gene flow. Demographic and temporal genetic data further indicates that flooding in rivers is unlikely to induce marked gene flow explaining the strong genetic differentiation at short geographical scale in such habitats. Finally, the demographic data suggest that some populations are transitory and subject to recurrent recolonization, a pattern that was also detected through genetic data.     

Genetic resilience of <Emphasis Type="Italic">Daphnia</Emphasis> populations following experimental removal of introduced fish

Dramatic changes in environmental conditions or community composition may impose severe selective pressures on resident populations. These changes in the selective regime can lead to demographic bottlenecks or local extinction. The consequence of demographic contraction is often a reduction of standing genetic variation. Since the level of adaptive genetic variation in populations plays an important role in persistence and adaptive response, understanding genetic resilience and the time course for re-establishment of genetic diversity following demographic perturbations is a critical component of assessing the consequences of changing environments. The introduction of nonnative fish into historically fishless lakes is a particularly dramatic environmental change frequently contributing to demographic bottlenecks and local extinction of native populations. We examine the quantitative- and molecular-genetic recovery of two alpine populations of the zooplankton Daphnia melanica from the Sierra Nevada, California, USA. These populations were extirpated by introduced salmonids and subsequently re-established following the experimental removal of nonnative fish. We obtained data for nuclear and mitochondrial markers and conducted a common-garden experiment to assess the levels of molecular- and quantitative-genetic variation following experimental fish removal. Reestablished D. melanica populations attained levels of nuclear genetic diversity only slightly lower than surrounding fishless populations in the first year following fish removal and substantial mitochondrial and quantitative-genetic diversity within 8 years. This high level of genetic resilience was likely facilitated by multiple sources of genetic variation, including immigration from neighboring populations and hatching from a local reservoir of diapausing eggs. Our results highlight the genetic resilience of taxa with reservoirs of genetic variation in seed or egg banks.     

Extinction,recolonization, and the genetic structure of tidepool copepod populations

Summary Extinction and recolonization in metapopulations may either increase or decrease genetic differentiation among populations, but recent genetic models predict increased differentiation under most circumstances of recolonization. I examine this prediction empirically using tidepool populations of the marine tidepool copepodTigriopus californicus. The probability of extinction of tidepool populations was sufficiently high to invoke the model's predictions, but varied among populations. Nearly 75% of colonizing groups consisted of 10 or fewer individuals. The genetic effective size of colonizing groups might be as high as 18, depending on assumptions, but colonists probably originated from a subset of local populations. In contrast to my predictions, genetic differentiation was smaller among younger tidepool populations than among older populations on each of three rock outcrops, suggesting that genetic differentiation was reduced by metapopulation dynamics. The discrepancy between the prediction and the results may be explained by the unmet assumptions of classical metapopulation structure underlying the genetic models.     

Genetic diversity and population structure of invasive and native populations of Erigeron canadensis L.

小蓬草入侵地和原产地种群的遗传多样性和种群结构 外来入侵植物对全球生物多样性造成了危害。小蓬草(Erigeron canadensis L.)是危害最为严重的外来农业杂草之一,代表了洲际入侵的典型例子。本研究利用10个多态性SSR位点,分别对采自中国江苏和浙江省的入侵地和采自美国阿拉巴马州的原产地各5个种群、共计312个植株的基因型进行了遗传多样性和遗传结构分析。结果表明,江苏省和浙江省的入侵种群显示出与阿拉巴马州原产地种群相似的遗传多样性,表明入侵期间没有严重的遗传瓶颈。利用STRUCTURE对种群结构的分析结果显示,种群之间分化较低,在原产地和入侵范围内均只仅检测到两个基因群。在入侵种群中观察到的遗传多样性较高,表明在入侵初期可能存在多次引入或引入了遗传背景不同的繁殖体。上述研究为阐明小蓬草这一全球有害杂草在中国东部的入侵动态提供了新的证据。在防除实践中,应注意防范小蓬草入侵种群和本地种群之间的种子基因流传播,阻止除草剂抗性植株的引入和扩散。     

'Sax-sess'-- genetics of primary succession in a pioneer species on two parallel glacier forelands

The primary succession on glacier forelands is characterized by a sequence of early and late successional species, but whether there is also a chronosequence at the intraspecific, genetic level is a matter of debate. Two opposing hypotheses differ in their prediction of genetic diversity in colonizing populations due to founder effects and postcolonization gene immigration. The development of genetic diversity in the pioneer Saxifraga aizoides was investigated along a successional gradient on two parallel glacier forelands, in order to test whether populations from older successional stages were less genetically diverse than populations from younger successional stages, and to locate the sources of the propagules that originally colonized new glacier foreland. Genetic diversity was determined with amplified fragment length polymorphisms, and potential sources of colonizing propagules were assessed via assignment tests. Our results indicate considerable postcolonization gene flow among populations on glacier forelands, since population differentiation was low and genetic diversity within populations was significantly higher. Molecular diversity and differentiation of populations did not develop linearly. Dispersal events within the glacier foreland, from the adjacent valley slopes, and from parallel glacier valleys were identified. In summary, it seems that the colonization of glacier forelands in the European Alps is highly dynamic and stochastic.     

Functional genomics of life history variation in a butterfly metapopulation

In fragmented landscapes, small populations frequently go extinct and new ones are established with poorly understood consequences for genetic diversity and evolution of life history traits. Here, we apply functional genomic tools to an ecological model system, the well-studied metapopulation of the Glanville fritillary butterfly. We investigate how dispersal and colonization select upon existing genetic variation affecting life history traits by comparing common-garden reared 2-day adult females from new populations with those from established older populations. New-population females had higher expression of abdomen genes involved in egg provisioning and thorax genes involved in the maintenance of flight muscle proteins. Physiological studies confirmed that new-population butterflies have accelerated egg maturation, apparently regulated by higher juvenile hormone titer and angiotensin converting enzyme mRNA, as well as enhanced flight metabolism. Gene expression varied between allelic forms of two metabolic genes (Pgi and Sdhd), which themselves were associated with differences in flight metabolic rate, population age and population growth rate. These results identify likely molecular mechanisms underpinning life history variation that is maintained by extinction-colonization dynamics in metapopulations.