The origins of postmating reproductive isolation: testing hypotheses in the grasshopper <Emphasis Type="Italic">Chorthippus parallelus</Emphasis>

 Although there are several well-established hypotheses for the origins of postmating isolation during allopatric divergence, there have been very few attempts to determine their relative importance in nature. We have developed an approach based on knowledge of the differing evolutionary histories of populations within species that allows systematic comparison of the predictions of these hypotheses. In previous work, we have applied this methodology to mating signal variation and premating reproductive isolation between populations of the meadow grasshopper Chorthippus parallelus. Here we review the principles behind our approach and report a study measuring postmating isolation in the same set of populations. The populations have known and differing evolutionary histories and relationships resulting from the colonization of northern Europe following the last glaciation. We use a maximum-likelihood analysis to compare the observed pattern of postmating isolation with the predictions of the hypotheses that isolation primarily evolves either as a result of gradual accumulation of mutations in allopatry, or through processes associated with colonization, such as founder events. We also quantify the extent to which degree of postmating isolation can be predicted by genetic distance. Our results suggest that although there is only a weak correlation between genetic distance and postmating isolation, long periods of allopatry do lead to postmating isolation. In contrast to the pattern of premating isolation described in our previous study, colonization does not seem to be associated with increased postmating isolation. Received: January 24, 2002 / Accepted: July 26, 2002 Acknowledgments Numerous people helped with collecting and rearing grasshoppers. We are grateful to NERC for funding. Correspondence to:R.K. Butlin     

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.     

Genetics of behavioural and morphological differences between parapatric subspecies of Chorthippus parallelus (Orthoptera: Acrididae)

The grasshoppers Chorthippus parallelus parallelus and C. p. erythropus form a narrow hybrid zone in the Pyrenees. They differ in several characters of the pattern and structure of male stridulation and in the morphology of the stridulatory file. These characters are considered to be involved in the species' mate recognition system.
Crosses have been made between a Pyrenean C. p. erythropus population and two C. p. parallelus populations, one in the Pyrenees and one in the Massif Central. Reciprocal Fls and backcrosses have been examined for a set of stridulation and associated morphological characters. The crosses confirm that the subspecific differences have a genetic basis and suggest that they are polygenically determined. However the mode of inheritance is not simple. There is evidence for dominance and epistatic effects and for sex-linkage or maternal effects. Genetic correlations exist between some pairs of characters in the backcrosses.
These results are discussed in the context of the hybrid zone and in relation to the general problem of the evolutionary divergence of mate recognition systems.     

The origins of premating reproductive isolation: testing hypotheses in the grasshopper Chorthippus parallelus

There are many proposed routes for the origin of premating reproductive isolation, but few systematic studies aimed at testing their relative importance. Accumulated information about the biogeographical history of the European meadow grasshopper, Chorthippus parallelus, has allowed us to make a planned series of comparisons among populations aimed at distinguishing the contributions of some of these hypotheses. We have compared the effects on assortative mating of long-term isolation in glacial refugia, founder events during postglacial colonization, and sympatry with a closely related species. A likelihood-based analysis allowed us to separate effects of variation in male and female mating propensity among populations from variation in mate choice leading to assortative mating. All three effects contributed significantly to the overall variation in mating pattern in a set of 21 pairwise comparisons among seven populations. Male cuticular composition, but not other candidate signals, was significantly associated with the level of assortative mating. Of the hypotheses for the origin of reproductive isolation, only the predictions of the founder hypothesis explained a significant amount of the variation in assortative mating. This does not rule out the possiblity that there may be some other explanation. Having established the pattern of divergence, it is possible to generate hypotheses that explain our results at least as well as the founder hypothesis. However, because many such post hoc hypotheses are possible, they cannot be tested with this dataset. On this basis, our results favor the hypothesis that some aspect of the colonization process tends to accelerate divergence in mating signals leading to premating reproductive isolation. This could be accomplished through any one of several mechanisms. Colonization involves many bottlenecks as new populations are established at the edge of the range by long-distance migrants. Genetic effects may be important, but these bottlenecks may also alter the conditions under which mates are found and chosen, as suggested by Kaneshiro. At the same time, the colonizing populations may encounter novel environmental challenges.     

Reconstructing the history of founder events using genome-wide patterns of allele sharing across individuals

Founder events play a critical role in shaping genetic diversity, fitness and disease risk in a population. Yet our understanding of the prevalence and distribution of founder events in humans and other species remains incomplete, as most existing methods require large sample sizes or phased genomes. Thus, we developed ASCEND that measures the correlation in allele sharing between pairs of individuals across the genome to infer the age and strength of founder events. We show that ASCEND can reliably estimate the parameters of founder events under a range of demographic scenarios. We then apply ASCEND to two species with contrasting evolutionary histories: ~460 worldwide human populations and ~40 modern dog breeds. In humans, we find that over half of the analyzed populations have evidence for recent founder events, associated with geographic isolation, modes of sustenance, or cultural practices such as endogamy. Notably, island populations have lower population sizes than continental groups and most hunter-gatherer, nomadic and indigenous groups have evidence of recent founder events. Many present-day groups––including Native Americans, Oceanians and South Asians––have experienced more extreme founder events than Ashkenazi Jews who have high rates of recessive diseases due their known history of founder events. Using ancient genomes, we show that the strength of founder events differs markedly across geographic regions and time––with three major founder events related to the peopling of Americas and a trend in decreasing strength of founder events in Europe following the Neolithic transition and steppe migrations. In dogs, we estimate extreme founder events in most breeds that occurred in the last 25 generations, concordant with the establishment of many dog breeds during the Victorian times. Our analysis highlights a widespread history of founder events in humans and dogs and elucidates some of the demographic and cultural practices related to these events.     

Genome-wide signatures of population bottlenecks and diversifying selection in European wolves

Genomic resources developed for domesticated species provide powerful tools for studying the evolutionary history of their wild relatives. Here we use 61K single-nucleotide polymorphisms (SNPs) evenly spaced throughout the canine nuclear genome to analyse evolutionary relationships among the three largest European populations of grey wolves in comparison with other populations worldwide, and investigate genome-wide effects of demographic bottlenecks and signatures of selection. European wolves have a discontinuous range, with large and connected populations in Eastern Europe and relatively smaller, isolated populations in Italy and the Iberian Peninsula. Our results suggest a continuous decline in wolf numbers in Europe since the Late Pleistocene, and long-term isolation and bottlenecks in the Italian and Iberian populations following their divergence from the Eastern European population. The Italian and Iberian populations have low genetic variability and high linkage disequilibrium, but relatively few autozygous segments across the genome. This last characteristic clearly distinguishes them from populations that underwent recent drastic demographic declines or founder events, and implies long-term bottlenecks in these two populations. Although genetic drift due to spatial isolation and bottlenecks seems to be a major evolutionary force diversifying the European populations, we detected 35 loci that are putatively under diversifying selection. Two of these loci flank the canine platelet-derived growth factor gene, which affects bone growth and may influence differences in body size between wolf populations. This study demonstrates the power of population genomics for identifying genetic signals of demographic bottlenecks and detecting signatures of directional selection in bottlenecked populations, despite their low background variability.     

A test of founder effect speciation using multiple loci in the auklets (Aethia spp.)

Whether speciation results more frequently from the genetic consequences of founder events or from gradual genetic divergence of large populations is a matter of debate. In this study, multiple analyses were applied to data from three loci (cytochrome b, alpha-enolase intron VIII, and MHC class II B) to test for founder effects associated with speciation in Aethia (Aves: Alcidae), a genus of seabirds thought to have undergone a rapid founder-induced radiation. Effective population sizes (N(e)) were derived from estimators of based on allelic diversity and the coalescent and from data on trans-species polymorphism. Results indicated that N(e) has been on the order of 10(5)-10(6) individuals throughout the evolutionary histories of least and crested auklets (A. pusilla and A. cristatella, respectively) and that N(e) of the ancestral species was at least 16,000 individuals. Computer simulations of MHC evolution indicated that a single-generation bottleneck at speciation could not have involved <85 individuals for each species. More moderate simulation scenarios indicated that population size could not have dropped below 2000 individuals at the time of species founding. Demographic history appears to have been stable for the auklets throughout the past several million years, and a founder effect associated with their speciation is unlikely.     

Comparative phylogeography of West African amphibians and reptiles

Comparative phylogeographic studies often support shared divergence times for co-distributed species with similar life histories and habitat specializations. During the late Holocene, West Africa experienced aridification and the turnover of rain forest habitats into savannas. These fragmented rain forests harbor impressive numbers of endemic and threatened species. In this setting, populations of co-distributed rain forest species are expected to have diverged simultaneously, whereas divergence events for species adapted to savanna and forest-edge habitats should be absent or idiosyncratic. We conducted a Bayesian analysis of shared evolutionary events to test models of population divergence for 20 species of anurans (frogs) and squamates (lizards and snakes) that are distributed across the Dahomey Gap, a climate change-induced savanna barrier responsible for fragmenting previously contiguous rain forests of Ghana into two regions: the Togo-Volta Hills and the Southwestern Forests. A model of asynchronous diversification is supported for anurans and squamates, suggesting that drivers of diversification are not specifically related to ecological and life history associations with habitat types. Instead, the wide variability of genetic divergence histories exhibited by these species suggests that biodiversity in this region has been shaped by diversification events that extend beyond the Holocene. Comparisons of the genealogical divergence index, a measure of the genetic divergence between populations due to the combined effects of genetic isolation and gene flow, illustrate that these populations represent a broad sampling of the speciation continuum.     

The origin of the Chorthippus parallelus hybrid zone: chromosomal evidence of multiple refugia for Iberian populations

A study of the variation in pattern and frequency of constitutive heterochromatin and nucleolar organizing regions of the X chromosomes of male Chorthippus parallelus grasshoppers in 25 populations within the Iberian peninsula requires us to revise our interpretation of the biogeography and evolutionary history of this species. Hybridization between the subspecies Cp erythropus and Cp parallelus, previously only known from populations in the Pyrenean cols, is shown to extend at least 400 km further into north-west Spain. A novel X-chromosome variant is described that appears to be close to fixation in 18 populations, mainly from the centre and south of Spain. Our findings indicate a possible independent origin for each of three distinct, nonderivative X variants present in Spain: the northern Cp erythropus and Cp parallelus variants, and a central-southern Cp erythropus variant. The first two are distinguished by interstitial and distal C bands, respectively, whereas the central-southern form has neither. This central-southern form is probably the current representative of the ancestral Iberian X variant. The pattern of variation supports the hypotheses of multiple refugia for Iberian populations and that more hybrid zones exist between these chromosomal variants.     

Colonization, extinction, and phylogeographic patterning in a freshwater crustacean

Phylogeographic analyses have revealed the importance of Pleistocene vicariance events in shaping the distribution of genetic diversity in freshwater fishes. However, few studies have examined the patterning of variation in freshwater organisms with differing dispersal syndromes and life histories. The present investigation addresses this gap, examining the phylogeography of Sida crystallina, a species whose production of diapausing eggs capable of passive dispersal was thought to constrain its regional genetic differentiation. By contrast, the present analysis has revealed deep allozyme and cytochrome oxidase I mitochondrial DNA divergence between populations from North America and Europe. Moreover, North American populations are separated into four allopatric assemblages, whose distribution suggests their derivation from different Pleistocene refugia. These lineages show higher haplotype diversity and deeper sequence divergence than those of any fish from temperate North America. Its distinctive life history traits have evidently sheltered lineages of Sida from extinction, contributing to a remarkably comprehensive and high resolution phylogeographic record.     

THE CHANGING PACE OF INSULAR LIFE: 5000 YEARS OF MICROEVOLUTION IN THE ORKNEY VOLE (MICROTUS ARVALIS ORCADENSIS)

Island evolution may be expected to involve fast initial morphological divergence followed by stasis. We tested this model using the dental phenotype of modern and ancient common voles (Microtus arvalis), introduced onto the Orkney archipelago (Scotland) from continental Europe some 5000 years ago. First, we investigated phenotypic divergence of Orkney and continental European populations and assessed climatic influences. Second, phenotypic differentiation among Orkney populations was tested against geography, time, and neutral genetic patterns. Finally, we examined evolutionary change along a time series for the Orkney Mainland. Molar gigantism and anterior‐lobe hypertrophy evolved rapidly in Orkney voles following introduction, without any transitional forms detected. Founder events and adaptation appear to explain this initial rapid evolution. Idiosyncrasy in dental features among different island populations of Orkney voles is also likely the result of local founder events following Neolithic translocation around the archipelago. However, against our initial expectations, a second marked phenotypic shift occurred between the 4th and 12th centuries AD, associated with increased pastoral farming and introduction of competitors (mice and rats) and terrestrial predators (foxes and cats). These results indicate that human agency can generate a more complex pattern of morphological evolution than might be expected in island rodents.     

Cryptic speciation in two widespread subterranean amphipod genera reflects historical drainage patterns in an ancient landscape

The landscape of the Pilbara region of Western Australia has been relatively unchanged for 100 million years. The ancient river systems of this region might be expected to be sources of isolation and divergence for aquatic species. Hence, the occurrence of widespread groundwater taxa in this landscape offers the opportunity to examine associations between genetic diversity and drainage patterns. Pilbarus and Chydaekata are two widespread genera of subterranean amphipods endemic to the Pilbara, each occupying multiple tributaries. We used molecular data to examine the roles of drainage patterns in structuring genetic diversity. Gene flow within a tributary may be facilitated by the occasional occurrence of these amphipods in springs, which results in their downstream dispersal during episodic flooding. However, tributary boundaries may form hydrological barriers to gene flow, resulting in localised isolation of populations and divergence. Samples of both genera, collected throughout three river basins, were examined for sequence divergence in the cytochrome c oxidase I mitochondrial gene. There was no evidence of contemporary gene flow among populations of either genus, and each tributary contained highly divergent lineages, which were not associated with similar morphological differentiation. This suggests cryptic speciation has occurred, and similar phylogenetic signals in both taxa imply similar evolutionary histories. Surface populations may have been driven into subterranean refugia by the cessation of flow in the rivers, associated with Tertiary climate change, while morphological evolution may have been constrained by stabilising selection. The lack of congruence between molecular diversity and morphology raises important practical issues for conservation.     

Contrasting phylogeographical patterns for springtails reflect different evolutionary histories between the Antarctic Peninsula and continental Antarctica

Aim  We examined the genetic structure among populations and regions for the springtails Cryptopygus antarcticus antarcticus and Gomphiocephalus hodgsoni (Collembola) to identify potential historical refugia and subsequent colonization routes, and to examine population growth/expansion and relative ages of population divergence.
Location  Antarctic Peninsula for C. a. antarcticus ; Antarctic continent (southern Victoria Land) for G. hodgsoni .
Methods  Samples were collected from 24 and 28 locations across the Antarctic Peninsula and southern Victoria Land regions for C. a. antarcticus and G. hodgsoni , respectively. We used population genetic, demographic and nested clade analyses based on mitochondrial DNA (cytochrome c oxidase subunit I and subunit II).
Results  Both species were found to have population structures compatible with the presence of historical glacial refugia on Pleistocene (2 Ma–present) time-scales, followed by post-glacial expansion generating contemporary geographically isolated populations. However, G. hodgsoni populations were characterized by a fragmented pattern with several 'phylogroups' (likely ancestral haplotypes present in high frequency) retaining strong ancestral linkages among present-day populations. Conversely, C. a. antarcticus had an excess of rare haplotypes with a much reduced volume of ancestral lineages, possibly indicating historical founder/bottleneck events and widespread expansion.
Main conclusions  We infer that these differences reflect distinct evolutionary histories in each locality despite the resident species having similar life-history characteristics. We suggest that this has predominantly been influenced by variation in the success of colonization events as a result of intrinsic historical glaciological differences between the Antarctic Peninsula and continental Antarctic environments.     

Adaptive life-history evolution in the livebearing fish Brachyrhaphis rhabdophora: genetic basis for parallel divergence in age and size at maturity and a test of predator-induced plasticity

I document a genetic basis for parallel evolution of life-history phenotypes in the livebearing fish Brachyrhaphis rhabdophora from northwestern Costa Rica. In previous work, I showed that populations of B. rhabdophora that co-occur with predators attain maturity at smaller sizes than populations that live in predator-free environments. I also demonstrated that this pattern of phenotypic divergence in life histories was independently repeated in at least five isolated drainages. However, life-history phenotypes measured from wild-caught fish could be attributed to environmental effects rather than to genetic differences among populations. In the present study, I reared male fish from four populations (two that co-occur with predators and two from predator-free environments) under four sets of environmental conditions. The pattern of phenotypic divergence in maturation size documented in the field between populations collected from different predation environments persisted after two generations in the laboratory. I also found a genetic basis for differences between populations in the age at which males attain maturity and in growth rates. By rearing fish in four different common environments, I tested for phenotypic plasticity in male life-history traits in response to nonlethal exposure to predators. There was a significant delay in the onset of sexual maturity in fish exposed to predators relative to those in the control, but no differences among treatments in size at maturity or growth rates. These results, coupled with previous work on B. rhabdophora, demonstrate a repeated pattern of parallel evolutionary divergence among genetically isolated populations that is strongly associated with predation.     

FOUNDER EFFECTS AND THE RATE OF MITOCHONDRIAL DNA EVOLUTION IN HAWAIIAN DROSOPHILA

The nearly-neutral-mutation theory predicts that populations with small effective sizes will undergo more rapid molecular evolution than populations with very large effective sizes. In particular, Ohta (1976) predicted that populations of Hawaiian Drosophila that are known to have small population sizes and to experience repeated population bottlenecks due to founder events should show a more rapid rate of molecular evolution relative to the rate of molecular evolution of species with large population sizes such as the continental Drosophila. In this paper we test this prediction by comparing the rate of molecular evolution in two closely related lineages of Hawaiian Drosophila that have experienced very different evolutionary histories. Both lineages belong to the planitibia subgroup of Hawaiian Drosophila. The beta lineage (which includes D. silvestris, D. planitibia, D. differens, and D. hemipeza) has undergone repeated founder events, as evidenced by their geographic distribution and behavioral biology. On the other hand, evidence on geographic distribution and behavior indicates that the alpha lineage (which includes D. melanocephala, D. cyrtaloma, and D. neoperkinsi) has arisen from large ancestral populations without founder effects. The mitochondrial DNA data reveal that, within a lineage, the rate of molecular evolution is rather uniform, while all comparisons between the two lineages show that the rate of molecular evolution in the beta lineage is three times that of the alpha lineage. This analysis strongly supports the predictions made by Ohta.     

Demographic history has shaped the strongly differentiated corkwing wrasse populations in Northern Europe

Understanding the biological processes involved in genetic differentiation and divergence between populations within species is a pivotal aim in evolutionary biology. One particular phenomenon that requires clarification is the maintenance of genetic barriers despite the high potential for gene flow in the marine environment. Such patterns have been attributed to limited dispersal or local adaptation, and to a lesser extent to the demographic history of the species. The corkwing wrasse (Symphodus melops) is an example of a marine fish species where regions of particular strong divergence are observed. One such genetic break occurred at a surprisingly small spatial scale (F_ST ~0.1), over a short coastline (<60 km) in the North Sea‐Skagerrak transition area in southwestern Norway. Here, we investigate the observed divergence and purported reproductive isolation using genome resequencing. Our results suggest that historical events during the post‐glacial recolonization route can explain the present population structure of the corkwing wrasse in the northeast Atlantic. While the divergence across the break is strong, we detected ongoing gene flow between populations over the break suggesting recent contact or negative selection against hybrids. Moreover, we found few outlier loci and no clear genomic regions potentially being under selection. We concluded that neutral processes and random genetic drift e.g., due to founder events during colonization have shaped the population structure in this species in Northern Europe. Our findings underline the need to take into account the demographic process in studies of divergence processes.     

EXPERIMENTAL EVIDENCE FOR THE EVOLUTION OF THE MAMMALIAN BACULUM BY SEXUAL SELECTION

Male genitalia exhibit a taxonomically widespread pattern of rapid and divergent evolution. Sexual selection is generally believed to be responsible for these patterns of evolutionary divergence, although empirical support for the sexual selection hypothesis comes mainly from studies of insects. Here we show that sexual selection is responsible for an evolutionary divergence in baculum morphology among populations of house mice Mus domesticus. We sourced mice from three isolated populations known to be subject to differing strengths of postcopulatory sexual selection and bred them under common‐garden conditions. Mice from populations with strong postcopulatory sexual selection had bacula that were relatively thicker compared with mice from populations with weak selection. We used experimental evolution to determine whether these patterns of divergence could be ascribed to postcopulatory sexual selection. After 27 generations of experimental evolution, populations of mice subjected to postcopulatory sexual selection evolved bacula that were relatively thicker than populations subjected to enforced monogamy. Our data thereby provide evidence that postcopulatory sexual selection underlies an evolutionary divergence in the mammalian baculum and supports the hypothesis that sexual selection plays a general role in the evolution of male genital morphology across evolutionary diverse taxonomic groups.     

GENETIC CONSEQUENCES OF PASSIVE DISPERSAL IN POND-DWELLING COPEPODS

Pond-dwelling copepods have colonized habitats throughout North America after glaciers have receded. Most species are passively transported via resting eggs into new habitats. Colonists originating in a glacial refugium could lose some of the ancestral genetic diversity when they establish new populations and the attenuation may be substantial in populations far removed from the refugium due to multiple founder events. Genetic variation was measured in Heterocope septentrionalis from 27 populations at arctic sites near potential refugia and those more recently deglaciated to determine the effects of postglacial dispersal on patterns of genetic relatedness and diversity. Some populations were more distant, genetically, from others within the same site than those from other more distant sites. Eleven polymorphic enzyme loci were significantly more variable (F [1,294 df] = 5.94, P < 0.025) among individuals from populations near the Alaskan refuge than those at the eastern limit of their distribution. Because populations are typically extremely large and stable this loss of genetic diversity is attributed primarily to repeated founder events during colonization. This result suggests profound genetic changes may occur on a continental scale in passively dispersed copepods due to founder events alone. Their potential for divergence and speciation is greater than currently recognized.     

Phylogeography and historical demography of the anadromous fish Leucopsarion petersii in relation to geological history and oceanography around the Japanese Archipelago

Phylogeographical patterns of marine and diadromous organisms are often influenced by dynamic ocean histories. For example, the marine realm around the Japanese Archipelago is an interesting area for phylogeographical research because of the wide variation in the environments driven by repeated shifts in sea level in the Quaternary. We analysed mitochondrial cyt b gene and nuclear myh6 gene sequences for individuals collected from throughout the range of the anadromous fish Leucopsarion petersii to assess the lineage divergence, phylogeographical pattern and historical demography in relation to geological history and oceanographic features around the archipelago. Leucopsarion petersii has two major lineages (the Japan Sea and Pacific Ocean lineages), which diverged during the late-early to middle Pleistocene. Geographical distributions of the two lineages were closely related to the pathways of the two warm currents, the Tsushima Current and the Kuroshio Current, that flow past the archipelago. Evidence of introgressive hybridization between these lineages was found at two secondary contact zones. Demographic tests suggested that the Japan Sea and Pacific Ocean lineages carried the genetic signal of different historical demographic processes, and these signals are probably associated with differences in habitat stability during recent glacial periods. The Japan Sea lineage has a larger body-size and more vertebrae, probably in relation to severe habitat conditions through Pleistocene climatic oscillations. Thus, the two lineages have long independent evolutionary histories, and the phylogeographical structure and demography of this species have been influenced both by historical events and the present-day oceanography around the Japanese Archipelago.     

Invasion genetics of vendace (Coregonus albula (L.)) in the Inari‐Pasvik watercourse: revealing the origin and expansion pattern of a rapid colonization event

Species invasions can have wide‐ranging biological and socio‐economic effects and are generally unwanted by legislation. Identification of the source population as well as the ecology and genetics of both the invader population and the receiving community is of crucial importance. The rapid invasion of a small coregonid fish vendace (Coregonus albula) in a major northern European subarctic watercourse has resulted in a labile ecological situation in the receiving community. The ecological impact of the invasion has been thoroughly documented, but the genetics of the invasion remains to be explored. We analyzed the genetic diversity and divergence patterns among the two possible source populations from southern Finnish Lapland and three colonists populations within the Inari‐Pasvik watercourse using ten microsatellite loci in order to (i) identify the most likely source of the invasion, (ii) reveal the dispersal pattern and genetic structure of the secondary expansion, and (iii) to investigate whether the initial introduction and the secondary expansion were associated with founder effects. We revealed that repeated translocation of vendace from Lake Sinettäjärvi into a tributary lake of L. Inari in 1964–1966 is the most plausible source for the invasion. Both the initial introduction and the secondary expansion were found not to be associated with significant founder effects. The secondary expansion followed a stepping stone pattern and the source and colonist populations of this expansion have undergone rapid genetic divergence within a period of 15–35 years (ca. 8–17 generations). The rapid divergence may be contributed to lack of gene flow among the source and colonist populations due to the extensive hydroelectric damming in the watercourse. Multiple introductions and substantial genetic variation in combination with the boom‐and‐bust population development of the species thus likely counteracted the founder effects as well as fueled the rapid establishment and expansion of this species within the Inari‐Pasvik watercourse.