Bilateral Song Convergence in a Passerine Hybrid Zone: Genetics Contribute in One Species Only

Hybridization can drive the convergence of territorial and sexual signals. However, non-genetic processes such as competition, environment matching, or cultural transmission, also generate this pattern. We investigated the effect of hybridization on song convergence between two interspecifically territorial warblers in a moving hybrid zone. We confirmed song convergence in each species. Using an AFLP-based genetic index, we detected an effect of genetics on song convergence in Hippolais polyglotta, the expanding species. Evidence was weaker for H. icterina, the receding species. In moving zones, introgression is expected to be larger in the expanding species than in the receding. Thus, the asymmetric contribution of the genetic index to convergence was consistent with expectations for genetically determined traits in moving hybrid zones, and the observed introgression pattern of AFLP markers. However, the geographical location of individuals had an effect on song variation too when genetics was accounted for, suggesting that convergence also has non-genetic explanations. We examine the possible role of alternative processes to that of hybridization and discuss their conflicting effects on reinforcement and hybrid zone dynamics.     

Species distribution models contribute to determine the effect of climate and interspecific interactions in moving hybrid zones

Climate is a major factor delimiting species’ distributions. However, biotic interactions may also be prominent in shaping geographical ranges, especially for parapatric species forming hybrid zones. Determining the relative effect of each factor and their interaction of the contact zone location has been difficult due to the lack of broad scale environmental data. Recent developments in species distribution modelling (SDM) now allow disentangling the relative contributions of climate and species’ interactions in hybrid zones and their responses to future climate change. We investigated the moving hybrid zone between the breeding ranges of two parapatric passerines in Europe. We conducted SDMs representing the climatic conditions during the breeding season. Our results show a large mismatch between the realized and potential distributions of the two species, suggesting that interspecific interactions, not climate, account for the present location of the contact zone. The SDM scenarios show that the southerly distributed species, Hippolais polyglotta, might lose large parts of its southern distribution under climate change, but a similar gain of novel habitat along the hybrid zone seems unlikely, because interactions with the other species (H. icterina) constrain its range expansion. Thus, whenever biotic interactions limit range expansion, species may become ‘trapped’ if range loss due to climate change is faster than the movement of the contact zone. An increasing number of moving hybrid zones are being reported, but the proximate causes of movement often remain unclear. In a global context of climate change, we call for more interest in their interactions with climate change.     

Competition and predation models applied to the case of the sibling birds species ofHippolais in Burgundy

We study the case of two sibling species ofHippolais(Aves). Very little differences can be observed in the morphology of both species. The breeding area of these species are complementary. Roughly, one species breeds North and East of Europe (Hippolais icterina) while the other breeds South and West of Europe (Hippolais polyglotta). There exitst a narrow zone of sympatry passing through Burgundy. Since several years, it has been observed that this area of sympatry was moving in the North-East direction at a European scale. This means that progressivelyH. icterina is declining and is replaced byH. polyglotta. Some assumptions can be made in order to explain this evolution, for instance competition or predation. Series of observations concerning the diets of nestlings of both species have been realized. These observations show some differences in the diet compositions. The breeding success of the two species has been studied. Numerical simulations of a competition model taking into account the observed differences between the food types eaten by the two species are presented. These simulations do not explain the regression ofH. icterina. Then, we present numerical simulations of a predation model with one predator attacking the nestlings of both species. These simulations show that with time one of the two preys must extinct. Predation rather than competition seems to be the right explanation.     

A spatial model of interspecific competition and selective predation: The case of the two Hippolais

Mutual exclusion between congeneric species has been observed such as the case of the grey and red squirrels in Great Britain and the case of the twoHippolais warbler speciesHippolais icterina andH. polyglotta in Europe. This process can lead to the formation of an extinction wave which propagates. Two main assumptions are tested, competition and selective predation. The aim of this work is to present spatial models of these two processes. The animals of two species are assumed to move on a two dimensional array of spatial patches with local interactions of competition or of selective predation between them. We focus on the case of mutual exclusion. Initially, the two competing species occupy complementary areas in an array of spatial patches with a small common zone. Numerical simulations show that under particular conditions, one species gets extinct and the other invades the whole set of spatial patches. These simulations show that with time, the length of the overlapping zone stabilizes and moves at a constant velocity. The limit length of the overlapping band and the velocity of the extinction wave are found to be functions of the parameters of the models. We relate this general model to the case of two sibling species of birds:H. icterina andH. polyglotta.     

Diversity, distribution and exchange of blood parasites meeting at an avian moving contact zone

Research on contact zones has paid relatively little attention to host-parasite interactions, although these situations have important but different implications depending on whether one considers the host or the parasite's perspective. We investigated both the role of a host contact zone in parasite expansion and whether parasites could influence contact zone dynamics. We studied the diversity and the patterns of parasite exchange (genera Haemoproteus and Plasmodium) infecting two parapatric sibling passerines meeting at a moving contact zone in western Europe. We amplified and sequenced a fragment of the parasite cytochrome b gene. The expanding host harboured more diverse parasites, which might indicate a superior ability to face a diverse parasite fauna than the receding host. Prevalence was very high in both hosts, due to the frequent occurrence of two sister Haemoproteus lineages. Despite the recent movement of the contact zone, these two parasites fitted almost perfectly to the geographic range of their main host species. Yet, we found several cases of cross-species infection in sympatric areas and evidences of asymmetrical spreading of parasites from the expanding host towards the receding host. Altogether, our results suggest that the host contact zone mainly acts as a barrier to parasite expansion even if recurrent host shifts are observed. Besides, they also support the idea that parasite-mediated competition might contribute to the displacement of hosts' contact zones, thereby emphasizing the role of parasitism on the population dynamics of sympatric species.     

Genetic discontinuities and disequilibria in recently established populations of the plant pathogenic fungus Mycosphaerella fijiensis

Dispersal processes of fungal plant pathogens can be inferred from analysis of spatial genetic structures resulting from recent range expansion. The relative importance of long‐distance dispersal (LDD) events vs. gradual dispersal in shaping population structures depends on the geographical scale considered. The fungus Mycosphaerella fijiensis, pathogenic on banana, is an example of a recent worldwide epidemic. Founder effects in this species were detected at both global and continental scale, suggesting stochastic spread of the disease through LDD events. In this study, we analysed the structure of M. fijiensis populations in two recently (∼1979–1980) colonized areas in Costa Rica and Cameroon. Isolates collected in 10–15 sites distributed along a ∼250‐ to 300‐ km‐long transect in each country were analysed using 19 microsatellite markers. We detected low‐to‐moderate genetic differentiation among populations in both countries and isolation by distance in Cameroon. Combined with historical data, these observations suggest continuous range expansion at the scale of banana‐production area through gradual dispersal of spores. However, both countries displayed specific additional signatures of colonization: a sharp discontinuity in gene frequencies was observed along the Cameroon transect, while the Costa Rican populations seemed not yet to have reached genetic equilibrium. These differences in the genetic characteristics of M. fijiensis populations in two recently colonized areas are discussed in the light of historical data on disease spread and ecological data on landscape features.     

Long‐distance dispersal maximizes evolutionary potential during rapid geographic range expansion

Conventional wisdom predicts that sequential founder events will cause genetic diversity to erode in species with expanding geographic ranges, limiting evolutionary potential at the range margin. Here, we show that invasive European starlings (Sturnus vulgaris) in South Africa preserve genetic diversity during range expansion, possibly as a result of frequent long‐distance dispersal events. We further show that unfavourable environmental conditions trigger enhanced dispersal, as indicated by signatures of selection detected across the expanding range. This brings genetic variation to the expansion front, counterbalancing the cumulative effects of sequential founding events and optimizing standing genetic diversity and thus evolutionary potential at range margins during spread. Therefore, dispersal strategies should be highlighted as key determinants of the ecological and evolutionary performances of species in novel environments and in response to global environmental change.     

Postglacial recolonization shaped the genetic diversity of the winter moth (Operophtera brumata) in Europe

Changes in climate conditions, particularly during the Quaternary climatic oscillations, have long been recognized to be important for shaping patterns of species diversity. For species residing in the western Palearctic, two commonly observed genetic patterns resulting from these cycles are as follows: (1) that the numbers and distributions of genetic lineages correspond with the use of geographically distinct glacial refugia and (2) that southern populations are generally more diverse than northern populations (the “southern richness, northern purity” paradigm). To determine whether these patterns hold true for the widespread pest species the winter moth (Operophtera brumata), we genotyped 699 individual winter moths collected from 15 Eurasian countries with 24 polymorphic microsatellite loci. We find strong evidence for the presence of two major genetic clusters that diverged ~18 to ~22 ka, with evidence that secondary contact (i.e., hybridization) resumed ~ 5 ka along a well‐established hybrid zone in Central Europe. This pattern supports the hypothesis that contemporary populations descend from populations that resided in distinct glacial refugia. However, unlike many previous studies of postglacial recolonization, we found no evidence for the “southern richness, northern purity” paradigm. We also find evidence for ongoing gene flow between populations in adjacent Eurasian countries, suggesting that long‐distance dispersal plays an important part in shaping winter moth genetic diversity. In addition, we find that this gene flow is predominantly in a west‐to‐east direction, suggesting that recently debated reports of cyclical outbreaks of winter moth spreading from east to west across Europe are not the result of dispersal.     

Fine-scale genetic structure and marginal processes in an expanding population of Biscutella laevigata L. (Brassicaceae)

Evolutionary processes acting at the expanding margins of a species' range are still poorly understood. Genetic drift is considered prevalent in marginal populations, and the maintenance of genetic diversity during recolonization might seem puzzling. To investigate such processes, a fine-scale investigation of 219 individuals was performed within a population of Biscutella laevigata (Brassicaceae), located at the leading edge of its range. The survey used amplified fragment length polymorphisms (AFLPs). As commonly reported across the whole species distribution range, individual density and genetic diversity decreased along the local axis of recolonization of this expanding population, highlighting the enduring effect of the historical colonization on present-day diversity. The self-incompatibility system of the plant may have prevented local inbreeding in newly found patches and sustained genetic diversity by ensuring gene flow from established populations. Within the more continuously populated region, spatial analysis of genetic structure revealed restricted gene flow among individuals. The distribution of genotypes formed a mosaic of relatively homogenous patches within the continuous population. This pattern could be explained by a history of expansion by long-distance dispersal followed by fine-scale diffusion (that is, a stratified dispersal combination). The secondary contact among expanding patches apparently led to admixture among differentiated genotypes where they met (that is, a reshuffling effect). This type of dynamics could explain the maintenance of genetic diversity during recolonization.     

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.     

Contrasting effects of long distance seed dispersal on genetic diversity during range expansion

Currently many attempts are made to reconstruct the colonization history of plant species after the last ice age. A surprising finding is that during the colonization phase genetic diversity did not decrease as much as expected. In this paper we examine whether long distance seed dispersal events could play a role in the unexpected maintenance of genetic diversity during range expansion. This study is based on simulations carried out with a maternally inherited haploid locus using a cellular automaton. The simulations reveal a close relationship between the frequency of long distance seed dispersal events and the amount of genetic diversity preserved during colonization. In particular, when the colonized region is narrow, a complete loss of genetic diversity results from the occurrence of very rare long distance dispersal (LDD) events. We call this phenomenon the 'embolism effect'. However, slightly higher rates of LDD events reverse this effect, up to the point that diversity is better preserved than in a pure diffusion model. This phenomenon is linked to the reorganization of the genetic structure during colonization and is called the 'reshuffling effect'.     

A first step towards inferring levels of long-distance dispersal during past expansions

Improving the realism of spatially explicit demographic models is important for better inferring the history of past populations and for understanding the genetic bases of adaptation and speciation. One particular type of demographic event to take into account is long-distance dispersal (LDD). The goals of this study are to explore the impact of various levels of LDD on genetic diversity and to show to what extent LDD levels can be correctly inferred from multilocus data sets using an approximate Bayesian computation approach. We therefore incorporated LDD into a 2D stepping stone forward simulation framework coupled to a coalescent backward simulation step to generate genetic diversity at 100 microsatellite markers under various demographic conditions relevant to recent human evolution. Our results confirm that LDD considerably increases genetic diversity within demes and decreases levels of diversity between demes. By controlling the spatial occurrence of LDD, it appears that LDD events occurring during a phase of range expansion into new territories are more important in maintaining genetic diversity than those occurring in the wake of the expansion or when colonization is over. We also show that it is possible to infer whether LDD has occurred during a range expansion, but our results suggest that one can only approximately estimate the extent of LDD based on genetic summary statistics.     

Retention of gene diversity during the spread of a non‐native plant species

Spatial expansion, which is a crucial stage in the process to successful biological invasion, is anticipated to profoundly affect the magnitude and spatial distribution of genetic diversity in novel colonized areas. Here, we show that, contrasting common expectations, Pyrenean rocket (Sisymbrium austriacum), retained SNP diversity as this introduced plant species descended in the Meuse River Basin. Allele frequencies did not mirror between‐population distances along the predominant expansion axis. Reconstruction of invasion history based on the genotypes of historical herbarium specimens indicated no influence of additional introductions or multiple points of entry on this nongradual pattern. Assignment analysis suggested the admixture of distant upstream sources in recently founded downstream populations. River dynamics seem to have facilitated occasional long‐distance dispersal which brought diversity to the expansion front and so maintained evolutionary potential. Our findings highlight the merit of a historical framework in interpreting extant patterns of genetic diversity in introduced species and underscore the need to integrate long‐distance dispersal events in theoretical work on the genetic consequences of range expansion.     

Modularity along organism dispersal gradients challenges a prevailing view of abrupt transitions in animal landscape perception

A common property of landscapes and metacommunities is the occurrence of abrupt shifts in connectivity along gradients of individual dispersal abilities. Animals with short‐range dispersal capability perceive fragmented landscapes, but organisms moving across critical thresholds perceive continuous landscapes. This qualitative shift in landscape perception may determine several attributes of local communities and the dynamics of whole metacommunities. Modularity describes the existence in some communities of relatively high numbers of mutual connections favoring the movement of neighboring individuals (even when each individual is able to reach any patch in the landscape). Local patch linkages and metacommunity connectivity along gradients of dispersal ability have been reported frequently. However, the intermediate level of structure captured by modularity has not been considered. We evaluated landscape connectivity and modularity along gradients of individual dispersal abilities. Random landscapes with different degrees of cell aggregation and occupancy were simulated; we also analyzed ten real ecosystems. An expected, a shift in landscape connectivity was always detected; modularity consistently decreased gradually along dispersal gradients in both simulated networks and empirical landscapes. Neutral metacommunities within simulated landscapes demonstrated that modularity and connectivity may reflect landscape traits in the shaping of metacommunity diversity. Average beta‐diversity was strongly associated with modularity, particularly with low migration rates, while connectivity trends tracked changes in beta‐diversity at intermediate to high migrations rates. Consequently, while some species are able to perceive abrupt transitions in the landscape, many others probably experience a gradual continuum in landscape perception, contrary to predictions from previous analyses. Furthermore, the gradual behavior of modularity indicates that it may represent an exceptional early‐warning tool that measures system distance to tipping points. Our study highlights the multiple perceptions that different species may have of a single landscape and shows, for the first time, a theoretical and empirical relationship between landscape modularity, and metacommunity diversity.     

Pursuing glacier retreat: genetic structure of a rapidly expanding Larix decidua population

One of the greatest threats to the long-term viability of migrating plant species is the loss of genetic diversity due to founder effects. Populations can expand as a response to climate change, but it is uncertain if long-lived plant species can maintain sufficient genetic diversity at the leading edge of migrating populations. This study uses an expanding Larix decidua population investigated along a chronosequence at landscape (350 ha) and local (0.8 ha) scales to test whether accelerated migration as a result of climate warming has the potential to intensify genetic erosion. Nine SSR markers revealed similar genetic diversity among eight sub-populations along the chronosequence (overall H(e) = 0.73; SE=0.04). Sub-populations were not genetically differentiated and all sampled individuals (N=730) formed one major genetic cluster indicating homogenizing gene flow despite spatial genetic structure (SGS) up to 80 m. At the local scale, individuals at the leading edge [early successional sub-population (ESSP), N =140] and a sub-population at equilibrium [late successional sub-population (LSSP), N = 290] revealed high genetic diversity in largest-sized cohorts. SGS among juveniles occurred up to 30 m in LSSP but there was no structure in ESSP. Accordingly, a maximum likelihood paternity assignment revealed local gene dispersal in LSSP (2-48 m) and intermediate-to-long distance dispersal into ESSP (115-3132 m). The findings indicate intensive mixing of the genes in this expanding population instead of founder effects and support the view that genetic diversity can be maintained in a long-lived species during rapid population expansion driven by climate warming.     

Can limited dispersal or biotic interaction explain the declining abundance of the whelk,Morula marginalba,at the edge of its range?

The southern range limit of the planktotrophic, intertidal whelk, Morula marginalba, occurs immediately to the north of the south‐east Australian biogeographical barrier and we predict that its range may be limited by dispersal and biotic interactions. The barrier includes several hundred kilometers without suitable habitat and is the convergence zone of major ocean currents. Within the barrier region, along‐shore larval transport is expected to be erratic, with water moving offshore to form long‐lived eddies. Through comparison of central and range edge populations, we test for evidence of recruitment limitation and interspecific competition with the whelk, Haustrum vinosum, which occurs sympatrically at the range edge. We found similar levels of recruitment and allozyme genetic variation within centre and edge populations where H. vinosum was absent, implying that populations are strongly interconnected. Nevertheless, recruitment and abundance of M. marginalba were lower at its extreme range limit, where it occurs with H. vinosum. Indeed, we detected significant inverse correlations between the abundance of these species, although their habitat use was similar and they consumed similar prey. These lines of evidence suggest a restricted recruitment across the barrier limits the range of M. marginalba but emphasize that multiple factors may act to set species range limits. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 849–862.     

Genetic signatures of a range expansion in natura: when clones play leapfrog

The genetic consequences of range expansions have generally been investigated at wide geographical and temporal scales, long after the colonization event. A unique ecological system enabled us to both monitor the colonization dynamics and decipher the genetic footprints of expansion over a very short time period. Each year an epidemic of the poplar rust (Melampsora larici‐populina) expands clonally and linearly along the Durance River, in the Alps. The colonization dynamics observed in 2004 showed two phases with different genetic outcomes. Upstream, fast colonization maintained high genetic diversity. Downstream, the colonization wave progressively faltered, diversity eroded, and differentiation increased, as expected under recurrent founder events. In line with the high dispersal abilities of rust pathogens, we provide evidence for leapfrog dispersal of clones. Our results thus emphasize the importance of colonization dynamics in shaping spatial genetic structure in the face of high gene flow.     

Genetic signature of the colonisation dynamics along a coastal expansion front in the damselfly Coenagrion scitulum

1. Many insects are expanding their distribution range polewards as a result of climate change, which has been shown to be associated with founder effects leading to a reduction in genetic diversity and an increase in genetic differentiation. These spatial genetic patterns may arise from colonisation from a broad expansion front or a limited neighbourhood after a stepping stone model of dispersal. The temporal persistence of such founder effects are poorly understood, mainly because studies looking at the fine‐scale initial temporal dynamics of the genetic signature of a range expansion are rare. 2. Using microsatellite markers, we performed a detailed spatiotemporal genetic analysis of the range expanding damselfly Coenagrion scitulum (Rambur) along a coastal axis during the first years after colonisation. 3. A decrease was in (private) allelic richness when going northwards along the coastline, which is consistent with a scenario of cumulative founder events. In spite of the spatiotemporal dynamics in the observation records of the species along the coastline, the spatial genetic data indicated a major contribution from the broad expansion front during the colonisation of the coastline rather than a stepping‐stone colonisation process. 4. The fine‐scale temporal dynamics of the range expansion indicated the absence of persistent founder effects and instead showed considerable temporal instability in genetic indices at the more northern edge populations. This may be explained by genetic immigration and admixture from the broad expansion front in this active disperser.     

Phylogeography of the Rhabditis (Pellioditis) marina species complex: evidence for long-distance dispersal, and for range expansions and restricted gene flow in the northeast Atlantic

Pinpointing processes that structure the geographical distribution of genetic diversity of marine species and lead to speciation is challenging because of the lack of obvious dispersal barriers and the likelihood of substantial (passive) dispersal in oceans. In addition, cryptic radiations with sympatric distributions abound in marine species, challenging the allopatric speciation mechanism. Here, we present a phylogeographical study of the marine nematode species complex Rhabditis ( Pellioditis ) marina to investigate processes shaping genetic structure and speciation. Rhabditis ( P .) marina lives on decaying macroalgae in the intertidal, and may therefore disperse over considerable distances. Rhabditis ( P .) marina consists of several cryptic species sympatrically distributed at a local scale. Genetic variation in the COI gene was screened in 1362 specimens from 45 locations around the world. Two nuclear DNA genes (ITS and D2D3) were sequenced to infer phylogenetic species. We found evidence for ten sympatrically distributed cryptic species, seven of which show a strong genetic structuring. A historical signature showed evidence for restricted gene flow with occasional long-distance dispersal and range expansions pre-dating the last glacial maximum. Our data also point to a genetic break around the British Isles and a contact zone in the Southern Bight of the North Sea. We provide evidence for the transoceanic distribution of at least one cryptic species (PmIII) and discuss the dispersal capacity of marine nematodes. The allopatric distribution of some intraspecific phylogroups and of closely related cryptic species points to the potential for allopatric speciation in R. ( P .) marina .     

Shifting dispersal modes at an expanding species’ range margin

While it is generally recognized that noncontiguous (long‐distance) dispersal of small numbers of individuals is important for range expansion over large geographic areas, it is often assumed that colonization on more local scales proceeds by population expansion and diffusion dispersal (larger numbers of individuals colonizing adjacent sites). There are few empirical studies of dispersal modes at the front of expanding ranges, and very little information is available on dispersal dynamics at smaller geographic scales where we expect contiguous (diffusion) dispersal to be prevalent. We used highly polymorphic genetic markers to characterize dispersal modes at a local geographic scale for populations at the edge of the range of a newly invasive grass species (Brachypodium sylvaticum) that is undergoing rapid range expansion in the Pacific Northwest of North America. Comparisons of Bayesian clustering of populations, patterns of genetic diversity, and gametic disequilibrium indicate that new populations are colonized ahead of the invasion front by noncontiguous dispersal from source populations, with admixture occurring as populations age. This pattern of noncontiguous colonization was maintained even at a local scale. Absence of evidence for dispersal among adjacent pioneer sites at the edge of the expanding range of this species suggests that pioneer populations undergo an establishment phase during which they do not contribute emigrants for colonization of neighbouring sites. Our data indicate that dispersal modes change as the invasion matures: initial colonization processes appear to be dominated by noncontiguous dispersal from only a few sources, while contiguous dispersal may play a greater role once populations become established.