Serial founder effects and genetic differentiation during worldwide range expansion of monarch butterflies

Range expansions can result in founder effects, increasing genetic differentiation between expanding populations and reducing genetic diversity along the expansion front. However, few studies have addressed these effects in long-distance migratory species, for which high dispersal ability might counter the effects of genetic drift. Monarchs (Danaus plexippus) are best known for undertaking a long-distance annual migration in North America, but have also dispersed around the world to form populations that do not migrate or travel only short distances. Here, we used microsatellite markers to assess genetic differentiation among 18 monarch populations and to determine worldwide colonization routes. Our results indicate that North American monarch populations connected by land show limited differentiation, probably because of the monarch''s ability to migrate long distances. Conversely, we found high genetic differentiation between populations separated by large bodies of water. Moreover, we show evidence for serial founder effects across the Pacific, suggesting stepwise dispersal from a North American origin. These findings demonstrate that genetic drift played a major role in shaping allele frequencies and created genetic differentiation among newly formed populations. Thus, range expansion can give rise to genetic differentiation and declines in genetic diversity, even in highly mobile species.     

Serial founder effects during range expansion: a spatial analog of genetic drift

Range expansions cause a series of founder events. We show that, in a one-dimensional habitat, these founder events are the spatial analog of genetic drift in a randomly mating population. The spatial series of allele frequencies created by successive founder events is equivalent to the time series of allele frequencies in a population of effective size ke, the effective number of founders. We derive an expression for ke in a discrete-population model that allows for local population growth and migration among established populations. If there is selection, the net effect is determined approximately by the product of the selection coefficients and the number of generations between successive founding events. We use the model of a single population to compute analytically several quantities for an allele present in the source population: (i) the probability that it survives the series of colonization events, (ii) the probability that it reaches a specified threshold frequency in the last population, and (iii) the mean and variance of the frequencies in each population. We show that the analytic theory provides a good approximation to simulation results. A consequence of our approximation is that the average heterozygosity of neutral alleles decreases by a factor of 1-1/(2ke) in each new population. Therefore, the population genetic consequences of surfing can be predicted approximately by the effective number of founders and the effective selection coefficients, even in the presence of migration among populations. We also show that our analytic results are applicable to a model of range expansion in a continuously distributed population.     

Strong founder effects and low genetic diversity in introduced populations of Coqui frogs

The success of non-native species may depend on the genetic resources maintained through the invasion process. The Coqui ( Eleutherodactylus coqui ), a frog endemic to Puerto Rico, was introduced to Hawaii in the late 1980s via the horticulture trade, and has become an aggressive invader. To explore whether genetic diversity and population structure changed with the introduction, we assessed individuals from 15 populations across the Hawaiian Islands and 13 populations across Puerto Rico using six to nine polymorphic microsatellite loci and five dorsolateral colour patterns. Allelic richness ( R _T) and gene diversity were significantly higher in Puerto Rico than in Hawaii populations. Hawaii also had fewer colour patterns (two versus three to five per population) than Puerto Rico. We found no isolation by distance in the introduced range, even though it exists in the native range. Results suggest extensive mixing among frog populations across Hawaii, and that their spread has been facilitated by humans. Like previous research, our results suggest that Hawaiian Coquis were founded by individuals from sites around San Juan, but unlike previous research the colour pattern and molecular genetic data (nuclear and mtDNA) support two separate introductions, one on the island of Hawaii and one on Maui. Coquis are successful invaders in Hawaii despite the loss of genetic variation. Future introductions may increase genetic variation and potentially its range.     

Rapid microevolution during recent range expansion to harsh environments

Background

Adaptive evolution is one of the crucial mechanisms for organisms to survive and thrive in new environments. Recent studies suggest that adaptive evolution could rapidly occur in species to respond to novel environments or environmental challenges during range expansion. However, for environmental adaptation, many studies successfully detected phenotypic features associated with local environments, but did not provide ample genetic evidence on microevolutionary dynamics. It is therefore crucial to thoroughly investigate the genetic basis of rapid microevolution in response to environmental changes, in particular on what genes and associated variation are responsible for environmental challenges. Here, we genotyped genome-wide gene-associated microsatellites to detect genetic signatures of rapid microevolution of a marine tunicate invader, Ciona robusta, during recent range expansion to the harsh environment in the Red Sea.

Results

The Red Sea population was significantly differentiated from the other global populations. The genome-wide scan, as well as multiple analytical methods, successfully identified a set of adaptive genes. Interestingly, the allele frequency largely varied at several adaptive loci in the Red Sea population, and we found significant correlations between allele frequency and local environmental factors at these adaptive loci. Furthermore, a set of genes were annotated to get involved in local temperature and salinity adaptation, and the identified adaptive genes may largely contribute to the invasion success to harsh environments.

Conclusions

All the evidence obtained in this study clearly showed that environment-driven selection had left detectable signatures in the genome of Ciona robusta within a few generations. Such a rapid microevolutionary process is largely responsible for the harsh environmental adaptation and therefore contributes to invasion success in different aquatic ecosystems with largely varied environmental factors.

     

Host range expansion of an introduced insect pest through multiple colonizations of specialized clones

Asexuality confers demographic advantages to invasive taxa, but generally limits adaptive potential for colonizing of new habitats. Therefore, pre-existing adaptations and habitat tolerance are essential in the success of asexual invaders. We investigated these key factors of invasiveness by assessing reproductive modes and host-plant adaptations in the pea aphid, Acyrthosiphon pisum, a pest recently introduced into Chile. The pea aphid encompasses lineages differing in their reproductive mode, ranging from obligatory cyclical parthenogenesis to fully asexual reproduction. This species also shows variation in host use, with distinct biotypes specialized on different species of legumes as well as more polyphagous populations. In central Chile, microsatellite genotyping of pea aphids sampled on five crops and wild legumes revealed three main clonal genotypes, which showed striking associations with particular host plants rather than sampling locations. Phenotypic analyses confirmed their strong host specialization and demonstrated parthenogenesis as their sole reproductive mode. The genetic relatedness of these clonal genotypes with corresponding host-specialized populations from the Old World indicated that each clone descended from a particular Eurasian biotype, which involved at least three successful introduction events followed by spread on different crops. This study illustrates that multiple introductions of highly specialized clones, rather than local evolution in resource use and/or selection of generalist genotypes, can explain the demographic success of a strictly asexual invader.     

Patterns of genetic diversity reveal multiple introductions and recurrent founder effects during range expansion in invasive populations of Geranium carolinianum (Geraniaceae)

Genetic diversity, and thus the adaptive potential of invasive populations, is largely based on three factors: patterns of genetic diversity in the species'' native range, the number and location of introductions and the number of founding individuals per introduction. Specifically, reductions in genetic diversity (‘founder effects'') should be stronger for species with low within-population diversity in their native range and few introductions of few individuals to the invasive range. We test these predictions with Geranium carolinianum, a winter annual herb native to North America and invasive in China. We measure the extent of founder effects using allozymes and microsatellites, and ask whether this is consistent with its colonization history and patterns of diversity in the native range. In the native range, genetic diversity is higher and structure is lower than expected based on life history traits. In China, our results provide evidence for multiple introductions near Nanjing, Jiangsu province, with subsequent range expansion to the west and south. Patterns of genetic diversity across China reveal weak founder effects that are driven largely by low-diversity populations at the expansion front, away from the introduction location. This suggests that reduced diversity in China has resulted from successive founder events during range expansion, and that the loss of genetic diversity in the Nanjing area was mitigated by multiple introductions from diverse source populations. This has implications for the future of G. carolinianum in China, as continued gene flow among populations should eventually increase genetic diversity within the more recently founded populations.     

Fine-scale genetic structure arises during range expansion of an invasive gecko

Processes of range expansion are increasingly important in light of current concerns about invasive species and range shifts due to climate change. Theoretical studies suggest that genetic structuring may occur during range expansion. Ephemeral genetic structure can have important evolutionary implications, such as propagating genetic changes along the wave front of expansion, yet few studies have shown evidence of such structure. We tested the hypothesis that genetic structure arises during range expansion in Hemidactylus mabouia, a nocturnal African gecko recently introduced to Florida, USA. Twelve highly variable microsatellite loci were used to screen 418 individuals collected from 43 locations from four sampling sites across Florida, representing a gradient from earlier (～1990s) to very recent colonization. We found earlier colonized locations had little detectable genetic structure and higher allelic richness than more recently colonized locations. Genetic structuring was pronounced among locations at spatial scales of tens to hundreds of meters near the leading edge of range expansion. Despite the rapid pace of range expansion in this introduced gecko, dispersal is limited among many suitable habitat patches. Fine-scale genetic structure is likely the result of founder effects during colonization of suitable habitat patches. It may be obscured over time and by scale-dependent modes of dispersal. Further studies are needed to determine if such genetic structure affects adaptation and trait evolution in range expansions and range shifts.     

Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture

The arbuscular mycorrhizal fungus Glomus mosseae is commonly found in agricultural fields. The cosmopolitan species is found in Africa, Europe, America, Asia and Australia. Three hypotheses may explain this worldwide distribution: First, speciation occurred before the continents separated 120 Ma; second, the distribution is a result of human-mediated dispersal related to agriculture and finally, the morphologically defined species may encompass several local endemic species. To test these hypotheses, three genes were sequenced from 82 isolates of G. mosseae originating from six continents and the resulting sequences analysed for geographical subdivision and estimation of migration between continents. Coalescent analyses estimated divergence and age of mutations. Bayesian coalescent modelling was used to reveal important past population changes in the global population. The sequence data showed no geographical structure, with identical genotypes found on different continents. Coalescence analyses indicated a recent diversification in the species, and the data could be explained by a recent population expansion in G. mosseae . The results of this study suggest that speciation and the range expansion happened much later than continental spread and that human activity may have had a major impact on the dispersal and the population structure of the fungus.     

Extensive contiguous north–south range expansion of the original population of an invasive lizard in Florida

Florida has one of the two worst non-indigenous invasive species problems in the United States, and all such species are considered by statute to be a potential ecological problem. Unfortunately, little information is available about most of Florida's invasive species. Here, we provide information on range expansion of a population of one of the lesser-known species. The Palm Beach County, Florida, population of the northern curly-tailed lizard, Leiocephalus carinatus armouri, was examined for north–south expansion of its previously documented range. Observations were conducted as contiguous expansion outward from the previously known range. We found a substantial contiguous range expansion by a minimum of 46.3 km to the south and 34.1 km to the north. This species appears to be closely associated with coastal habitat degradation in the form of human infrastructure, especially ageing pavement, sea walls, buildings, and bridge bases.     

Low genetic and morphological differentiation between an introduced population of dunnocks in New Zealand and an ancestral population in England

Species invasions and exotic species introductions can be considered as ??unplanned experiments??, which help us to understand the evolution of organisms. In this study, we investigated whether an exotic bird species, the dunnock (Prunella modularis), has diverged genetically and morphologically from its native source population (Cambridge, England) after introduction into a new environment (Dunedin, South Island of New Zealand; exotic population). We used a set of microsatellite markers and three morphological traits to quantify the divergence between these two populations. We quantified neutral genotypic differentiation between the populations, and also used an individual-based Bayesian clustering method to assess genetic structure. We compared morphological divergence using univariate and principal components analyses. We found that individuals from the Dunedin population are genetically distinct from the Cambridge population, but levels of differentiation are very low. Overall within-population levels of genetic diversity are low compared to other bird species, and effective population sizes are small; indicating that the native population probably has a historically low level of genetic diversity, and that the introduced population retained most of that diversity after its introduction into New Zealand. We found little evidence of morphological divergence, and the evolutionary rate of change in these traits is below the average for other taxa. Our study adds support to the growing literature showing that invasive species maintain most of their initial genetic diversity after multiple founder events, even when population size is severely reduced. Moreover, our morphological data indicate slow evolutionary rates in species introduced to similar habitats.     

Modelling Allee effects in a transgenic mosquito population during range expansion

ABSTRACT

Mosquitoes are vectors for many diseases that cause significant mortality and morbidity. As mosquito populations expand their range, they may undergo mate-finding Allee effects such that their ability to successfully reproduce becomes difficult at low population density. With new technology, creating target specific gene modification may be a viable method for mosquito population control. We develop a mathematical model to investigate the effects of releasing transgenic mosquitoes into newly established, low-density mosquito populations. Our model consists of two life stages (aquatic and adults), which are divided into three genetically distinct groups: heterogeneous and homogeneous transgenic that cause female infertility and a homogeneous wild type. We perform analytical and numerical analyses on the equilibria to determine the level of saturation needed to eliminate mosquitoes in a given area. This model demonstrates the potential for a gene drive system to reduce the spread of invading mosquito populations.     

Re-creation of the genetic composition of a founder population

Human ethnic groups are frequently comprised of two or more founder populations. One of these founding populations is often available for contemporary sampling. We describe a method for reconstructing the composition of a missing founder population using the highly informative haplotypes comprising the HLA system. An application of the method is demonstrated using bone marrow registry samples of African Americans. We use contemporary samples of African Americans and European Americans to derive haplotypes of the West African founder populations. This approach may also be useful for reconstructing ancestral haplotypes for regions elsewhere in the genome.     

Congruent morphological and genetic differentiation as a signature of range expansion in a fragmented landscape

Phenotypic differentiation is often interpreted as a result of local adaptation of individuals to their environment. Here, we investigated the skull morphological differentiation in 11 populations of the white‐footed mouse (Peromyscus leucopus). These populations were sampled in an agricultural landscape in the Montérégie region (Québec, Canada), at the northern edge of the distribution of the white‐footed mouse. We found a strong pattern of phenotypic differentiation matching the genetic structure across these populations. Landscape fragmentation and the presence of geographic barriers, in particular north–south oriented rivers, contribute to this differentiation and modulate the pattern of rapid ongoing northward range expansion of the white‐footed mouse in response to climate warming. We conclude that while large rivers and postglacial recolonization routes have shaped the current pattern of distribution and differentiation of white‐footed mouse populations, further local differentiation is occurring, at the scale of the landscape. We posit that the northern expansion of the white‐footed mouse is achieved through successive independent founder events in a fragmented landscape at the northern range edge of the species. The phenotypic differentiation we observe is thus a result of a number of mechanisms operating at different spatial and temporal scales.     

Exploratory behaviour and stressor hyper-responsiveness facilitate range expansion of an introduced songbird

Global anthropogenic changes are occurring at an unprecedented rate; one change, human-facilitated introduction of species outside their native range, has had significant ecological and economic impacts. Surprisingly, what traits facilitate range expansions post-introduction is relatively unknown. This information could help predict future expansions of introduced species as well as native species shifting their ranges as climate conditions change. Here, we asked whether specific behavioural and physiological traits were important in the ongoing expansion of house sparrows (Passer domesticus) across Kenya. We predicted that birds at the site of initial introduction (Mombasa, introduced approx. 1950) would behave and regulate corticosterone, a stress hormone, differently than birds at the range edge (Kakamega, approx. 885 km from Mombasa; colonized within the last 5 years). Specifically, we predicted greater exploratory behaviour and stronger corticosterone response to stressors in birds at the range edge, which may facilitate the identification, resolution and memory of stressors. Indeed, we found that distance from Mombasa (a proxy for population age) was a strong predictor of both exploratory behaviour and corticosterone release in response to restraint (but only while birds were breeding). These results suggest that certain behavioural and neuroendocrine traits may influence the ability of species to colonize novel habitats.     

Admixture determines genetic diversity and population differentiation in the biological invasion of a lizard species

Molecular genetic analyses show that introduced populations undergoing biological invasions often bring together individuals from genetically disparate native-range source populations, which can elevate genotypic variation if these individuals interbreed. Differential admixture among multiple native-range sources explains mitochondrial haplotypic diversity within and differentiation among invasive populations of the lizard Anolis sagrei. Our examination of microsatellite variation supports the hypothesis that lizards from disparate native-range sources, identified using mtDNA haplotypes, form genetically admixed introduced populations. Furthermore, within-population genotypic diversity increases with the number of sources and among-population genotypic differentiation reflects disparity in their native-range sources. If adaptive genetic variation is similarly restructured, then the ability of invasive species to adapt to new conditions may be enhanced.     

Contemporary ecotypic divergence during a recent range expansion was facilitated by adaptive introgression

Although rapid phenotypic evolution during range expansion associated with colonization of contrasting habitats has been documented in several taxa, the evolutionary mechanisms that underlie such phenotypic divergence have less often been investigated. A strong candidate for rapid ecotype formation within an invaded range is the three‐spine stickleback in the Lake Geneva region of central Europe. Since its introduction only about 140 years ago, it has undergone a significant expansion of its range and its niche, now forming phenotypically differentiated parapatric ecotypes that occupy either the pelagic zone of the large lake or small inlet streams, respectively. By comparing museum collections from different times with contemporary population samples, we here reconstruct the evolution of parapatric phenotypic divergence through time. Using genetic data from modern samples, we infer the underlying invasion history. We find that parapatric habitat‐dependent phenotypic divergence between the lake and stream was already present in the first half of the twentieth century, but the magnitude of differentiation increased through time, particularly in antipredator defence traits. This suggests that divergent selection between the habitats occurred and was stable through much of the time since colonization. Recently, increased phenotypic differentiation in antipredator defence traits likely results from habitat‐dependent selection on alleles that arrived through introgression from a distantly related lineage from outside the Lake Geneva region. This illustrates how hybridization can quickly promote phenotypic divergence in a system where adaptation from standing genetic variation was constrained.     

Mitochondrial DNA analysis of Tunisians reveals a mosaic genetic structure with recent population expansion

Tunisia is a country of great interest for human population genetics due to its strategic geographic position and rich human settlement history. These factors significantly contributed to the genetic makeup of present-day Tunisians harbouring components of diverse geographic origins. Here, we investigated the genetic structure of Tunisians by performing a mitochondrial DNA (mtDNA) comparison of 15 Tunisian population groups, in order to explore their complex genetic landscape. All Tunisian data were also analysed against 40 worldwide populations. Statistical results (Tajima's D and Fu's F_S tests) suggested recent population expansion for the majority of studied populations, as well as showed (AMOVA test) that all populations were significantly different from each other, which is evidence of population structure even if it is not guided by geographic and ethnic effects. Gene flow analysis revealed the assignment of Tunisians to multiple ancestries, which agrees with their genetic heterogeneity. The resulting picture for the mtDNA pool confirms the evidence of a recent expansion of the Tunisian population and is in accordance with a mosaic structure, composed by North African, Middle Easterner, European and Sub-Saharan lineages, resulting from a complex settlement history.     

Rapid evolution of phenology during range expansion with recent climate change

Although climate warming is expected to make habitat beyond species’ current cold range edge suitable for future colonization, this new habitat may present an array of biotic or abiotic conditions not experienced within the current range. Species’ ability to shift their range with climate change may therefore depend on how populations evolve in response to such novel environmental conditions. However, due to the recent nature of thus far observed range expansions, the role of rapid adaptation during climate change migration is only beginning to be understood. Here, we evaluated evolution during the recent native range expansion of the annual plant Dittrichia graveolens, which is spreading northward in Europe from the Mediterranean region. We examined genetically based differentiation between core and edge populations in their phenology, a trait that is likely under selection with shorter growing seasons and greater seasonality at northern latitudes. In parallel common garden experiments at range edges in Switzerland and the Netherlands, we grew plants from Dutch, Swiss, and central and southern French populations. Population genetic analysis following RAD‐sequencing of these populations supported the hypothesized central France origins of the Swiss and Dutch range edge populations. We found that in both common gardens, northern plants flowered up to 4 weeks earlier than southern plants. This differentiation in phenology extended from the core of the range to the Netherlands, a region only reached from central France over approximately the last 50 years. Fitness decreased as plants flowered later, supporting the hypothesized benefits of earlier flowering at the range edge. Our results suggest that native range expanding populations can rapidly adapt to novel environmental conditions in the expanded range, potentially promoting their ability to spread.