Deciphering the worldwide invasion of the Asian long‐horned beetle: A recurrent invasion process from the native area together with a bridgehead effect

Retracing introduction routes is crucial for understanding the evolutionary processes involved in an invasion, as well as for highlighting the invasion history of a species at the global scale. The Asian long‐horned beetle (ALB) Anoplophora glabripennis is a xylophagous pest native to Asia and invasive in North America and Europe. It is responsible for severe losses of urban trees, in both its native and invaded ranges. Based on historical and genetic data, several hypotheses have been formulated concerning its invasion history, including the possibility of multiple introductions from the native zone and secondary dispersal within the invaded areas, but none have been formally tested. In this study, we characterized the genetic structure of ALB in both its native and invaded ranges using microsatellites. In order to test different invasion scenarios, we used an approximate Bayesian “random forest” algorithm together with traditional population genetics approaches. The strong population differentiation observed in the native area was not geographically structured, suggesting complex migration events that were probably human‐mediated. Both native and invasive populations had low genetic diversity, but this characteristic did not prevent the success of the ALB invasions. Our results highlight the complexity of invasion pathways for insect pests. Specifically, our findings indicate that invasive species might be repeatedly introduced from their native range, and they emphasize the importance of multiple, human‐mediated introductions in successful invasions. Finally, our results demonstrate that invasive species can spread across continents following a bridgehead path, in which an invasive population may have acted as a source for another invasion.     

Host population genetics and biogeography structure the microbiome of the sponge Cliona delitrix

Sponges occur across diverse marine biomes and host internal microbial communities that can provide critical ecological functions. While strong patterns of host specificity have been observed consistently in sponge microbiomes, the precise ecological relationships between hosts and their symbiotic microbial communities remain to be fully delineated. In the current study, we investigate the relative roles of host population genetics and biogeography in structuring the microbial communities hosted by the excavating sponge Cliona delitrix. A total of 53 samples, previously used to demarcate the population genetic structure of C. delitrix, were selected from two locations in the Caribbean Sea and from eight locations across the reefs of Florida and the Bahamas. Microbial community diversity and composition were measured using Illumina‐based high‐throughput sequencing of the 16S rRNA V4 region and related to host population structure and geographic distribution. Most operational taxonomic units (OTUs) specific to Cliona delitrix microbiomes were rare, while other OTUs were shared with congeneric hosts. Across a large regional scale (>1,000 km), geographic distance was associated with considerable variability of the sponge microbiome, suggesting a distance–decay relationship, but little impact over smaller spatial scales (<300 km) was observed. Host population structure had a moderate effect on the structure of these microbial communities, regardless of geographic distance. These results support the interplay between geographic, environmental, and host factors as forces determining the community structure of microbiomes associated with C. delitrix. Moreover, these data suggest that the mechanisms of host regulation can be observed at the population genetic scale, prior to the onset of speciation.     

Fine‐scale population structure of Collichtys lucidus populations inferred from microsatellite markers

The spinyhead croaker Collichthys lucidus (Richardson) is a small sciaenid species distributed along the inshore waters of northwestern Pacific Ocean, and now has been listed as Key Protected Commercial Sources of Aquatic Animals and Plants in China. To delineate stock boundaries and inform conservation policy for its management, samples were collected from eight locations across the Chinese coastal waters and analyzed at nine microsatellite loci. C. lucidus populations showed low genetic diversity (expected heterozygosity = 0.445–0.542; observed heterozygosity = 0.392–0.539; Polymorphism Information Content = 0.268–0.684). Strong genetic fdifferentiation (F_st = 0.065–0.510, all significant after Bonferroni correction) among all populations and high levels of self‐recruitment (89.2%–91.5%) were observed, which suggested limited genetic exchange for this species. Clustering results of discriminant analysis of principal components and STRUCTURE found strong support for obvious genetic clusters (populations FZ, XM and SZ vs. populations SH, YRE, ZS, WZ and ND). The results of the present study not only supported the phylogeographic pattern of north‐south differentiation, but also suggested that C. lucidus populations may be predominantly sustained by self‐replenishment rather than by recruitment from distant populations.     

Genetic assignment of recruits reveals short‐ and long‐distance larval dispersal in Pocillopora damicornis on the Great Barrier Reef

Understanding connectivity of coral populations among and within reefs over ecologically significant timescales is essential for developing evidence‐based management strategies, including the design of marineprotected areas. Here, we present the first assessment of contemporary connectivity among populations of two Molecular Operational Taxonomic Units (MOTUs) of the brooding coral Pocillopora damicornis. We used individual‐based genetic assignment methods to identify the proportions of philopatric and migrant larval recruits, settling over 12 months at sites around Lizard Island (northern Great Barrier Reef [GBR]) and over 24 months at sites around the Palms Islands (central GBR). Overall, we found spatially and temporally variable rates of self‐recruitment and dispersal, demonstrating the importance of variation in local physical characteristics in driving dispersal processes. Recruitment patterns and inferred dispersal distances differed between the two P. damicornis MOTUs, with type α recruits exhibiting predominantly philopatric recruitment, while the majority of type β recruits were either migrants from identified putative source populations or assumed migrants based on genetic exclusion from all known populations. While P. damicornis invests much energy into brooding clonal larvae, we found that only 15% and 7% of type α and type β recruits, respectively, were clones of sampled adult colonies or other recruits, challenging the hypothesis that reproduction is predominantly asexual in this species on the GBR. We explain high rates of self‐recruitment and low rates of clonality in these MOTUs by suggesting that locally retained larvae originate predominantly from spawned gametes, while brooded larvae are mainly vagabonds.     

Inferences on population history of a seed chalcid wasp: invasion success despite a severe founder effect from an unexpected source population

Most invasive species established in Europe originate from either Asia or North America, but little is currently known about the potential of the Anatolian Peninsula (Asia Minor) and/or the Near East to constitute invasion sources. Mediterranean forests are generally fragile ecosystems that can be threatened by invasive organisms coming from different regions of the Mediterranean Basin, but for which historical data are difficult to gather and the phylogeographic patterns are still poorly understood for most terrestrial organisms. In this study, we characterized the genetic structure of Megastigmus schimitscheki, an invasive seed‐feeding insect species originating from the Near East, and elucidated its invasion route in South‐eastern France in the mid 1990s. To disentangle the evolutionary history of this introduction, we gathered samples from the main native regions (Taurus Mountains in Turkey, Lebanon and Cyprus) and from the invaded region that we genotyped using five microsatellite markers and for which we sequenced the mitochondrial Cytochrome Oxidase I gene. We applied a set of population genetic statistics and methods, including approximate Bayesian computation. We proposed a detailed phylogeographic pattern for the Near East populations, and we unambiguously showed that the French invasive populations originated from Cyprus, although the available historical data strongly suggested that Turkey could be the most plausible source area. Interestingly, we could show that the introduced populations were founded from an extremely restricted number of individuals that realized a host switch from Cedrus brevifolia to C. atlantica. Evolutionary hypotheses are discussed to account for this unlikely scenario.     

Range‐wide population genetic structure of the Caribbean sea fan coral,Gorgonia ventalina

The population structure of benthic marine organisms is of central relevance to the conservation and management of these often threatened species, as well as to the accurate understanding of their ecological and evolutionary dynamics. A growing body of evidence suggests that marine populations can be structured over short distances despite theoretically high dispersal potential. Yet the proposed mechanisms governing this structure vary, and existing empirical population genetic evidence is of insufficient taxonomic and geographic scope to allow for strong general inferences. Here, we describe the range‐wide population genetic structure of an ecologically important Caribbean octocoral, Gorgonia ventalina. Genetic differentiation was positively correlated with geographic distance and negatively correlated with oceanographically modelled dispersal probability throughout the range. Although we observed admixture across hundreds of kilometres, estimated dispersal was low, and populations were differentiated across distances <2 km. These results suggest that populations of G. ventalina may be evolutionarily coupled via gene flow but are largely demographically independent. Observed patterns of differentiation corroborate biogeographic breaks found in other taxa (e.g. an east/west divide near Puerto Rico), and also identify population divides not discussed in previous studies (e.g. the Yucatan Channel). High genotypic diversity and absence of clonemates indicate that sex is the primary reproductive mode for G. ventalina. A comparative analysis of the population structure of G. ventalina and its dinoflagellate symbiont, Symbiodinium, indicates that the dispersal of these symbiotic partners is not coupled, and symbiont transmission occurs horizontally.     

Unexpectedly complex gradation of coral population structure in the Nansei Islands,Japan

To establish effective locations and sizes of potential protected areas for reef ecosystems, detailed information about source and sink relationships between populations is critical, especially in archipelagic regions. Therefore, we assessed population structure and genetic diversity of Acropora tenuis, one of the dominant stony coral species in the Pacific, using 13 microsatellite markers to investigate 298 colonies from 15 locations across the Nansei Islands in southwestern Japan. Genetic diversity was not significant among sampling locations, even in possibly peripheral locations. In addition, our results showed that there are at least two populations of A. tenuis in the study area. The level of genetic differentiation between these populations was relatively low, but significant between many pairs of sampling locations. Directions of gene flow, which were estimated using a coalescence‐based approach, suggest that gene flow not only occurs from south to north, but also from north to south in various locations. Consequently, the Yaeyama Islands and the Amami Islands are potential northern and southern sources of corals. On the other hand, the Miyako Islands and west central Okinawa Island are potential sink populations. The Kerama Islands and the vicinity of Taketomi Island are potential contact points of genetic subdivision of coral populations in the Nansei Islands. We found that genetic population structure of A. tenuis in the Nansei Islands is more complex than previously thought. These cryptic populations are very important for preserving genetic diversity and should be maintained.     

Sampling related individuals within ponds biases estimates of population structure in a pond‐breeding amphibian

Effective conservation and management of pond‐breeding amphibians depends on the accurate estimation of population structure, demographic parameters, and the influence of landscape features on breeding‐site connectivity. Population‐level studies of pond‐breeding amphibians typically sample larval life stages because they are easily captured and can be sampled nondestructively. These studies often identify high levels of relatedness between individuals from the same pond, which can be exacerbated by sampling the larval stage. Yet, the effect of these related individuals on population genetic studies using genomic data is not yet fully understood. Here, we assess the effect of within‐pond relatedness on population and landscape genetic analyses by focusing on the barred tiger salamanders (Ambystoma mavortium) from the Nebraska Sandhills. Utilizing genome‐wide SNPs generated using a double‐digest RADseq approach, we conducted standard population and landscape genetic analyses using datasets with and without siblings. We found that reduced sample sizes influenced parameter estimates more than the inclusion of siblings, but that within‐pond relatedness led to the inference of spurious population structure when analyses depended on allele frequencies. Our landscape genetic analyses also supported different models across datasets depending on the spatial resolution analyzed. We recommend that future studies not only test for relatedness among larval samples but also remove siblings before conducting population or landscape genetic analyses. We also recommend alternative sampling strategies to reduce sampling siblings before sequencing takes place. Biases introduced by unknowingly including siblings can have significant implications for population and landscape genetic analyses, and in turn, for species conservation strategies and outcomes.     

How relatedness between mates influences reproductive success: An experimental analysis of self‐fertilization and biparental inbreeding in a marine bryozoan

Kin associations increase the potential for inbreeding. The potential for inbreeding does not, however, make inbreeding inevitable. Numerous factors influence whether inbreeding preference, avoidance, or tolerance evolves, and, in hermaphrodites where both self‐fertilization and biparental inbreeding are possible, it remains particularly difficult to predict how selection acts on the overall inbreeding strategy, and to distinguish the type of inbreeding when making inferences from genetic markers. Therefore, we undertook an empirical analysis on an understudied type of mating system (spermcast mating in the marine bryozoan, Bugula neritina) that provides numerous opportunities for inbreeding preference, avoidance, and tolerance. We created experimental crosses, containing three generations from two populations to estimate how parental reproductive success varies across parental relatedness, ranging from self, siblings, and nonsiblings from within the same population. We found that the production of viable selfed offspring was extremely rare (only one colony produced three selfed offspring) and biparental inbreeding more common. Paternity analysis using 16 microsatellite markers confirmed outcrossing. The production of juveniles was lower for sib mating compared with nonsib mating. We found little evidence for consistent inbreeding, in terms of nonrandom mating, in adult samples collected from three populations, using multiple population genetic inferences. Our results suggest several testable hypotheses that potentially explain the overall mating and dispersal strategy in this species, including early inbreeding depression, inbreeding avoidance through cryptic mate choice, and differential dispersal distances of sperm and larvae.     

Differences in developmental strategies between long‐settled and invasion‐front populations of the cane toad in Australia

Phenotypic plasticity can enhance a species’ ability to persist in a new and stressful environment, so that reaction norms are expected to evolve as organisms encounter novel environments. Biological invasions provide a robust system to investigate such changes. We measured the rates of early growth and development in tadpoles of invasive cane toads (Rhinella marina) in Australia, from a range of locations and at different larval densities. Populations in long‐colonized areas have had the opportunity to adapt to local conditions, whereas at the expanding range edge, the invader is likely to encounter challenges that are both novel and unpredictable. We thus expected invasion‐vanguard populations to exhibit less phenotypic plasticity than range‐core populations. Compared to clutches from long‐colonized areas, clutches from the invasion front were indeed less plastic (i.e. rates of larval growth and development were less sensitive to density). In contrast, those rates were highly variable in clutches from the invasion front, even among siblings from the same clutch under standard conditions. Clutches with highly variable rates of growth and development under constant conditions had lower phenotypic plasticity, suggesting a trade‐off between these two strategies. Although these results reveal a strong pattern, further investigation is needed to determine whether these different developmental strategies are adaptive (i.e. adaptive phenotypic plasticity vs. bet‐hedging) or instead are driven by geographic variation in genetic quality or parental effects.     

Phylogeographic insights into the invasion history and secondary spread of the signal crayfish in Japan

Successful invasion by nonindigenous species is often attributed to high propagule pressure, yet some foreign species become widespread despite showing reduced genetic variation due to founder effects. The signal crayfish (Pacifastacus leniusculus) is one such example, where rapid spread across Japan in recent decades is believed to be the result of only three founding populations. To infer the history and explore the success of this remarkable crayfish invasion, we combined detailed phylogeographical and morphological analyses conducted in both the introduced and native ranges. We sequenced 16S mitochondrial DNA of signal crayfish from across the introduced range in Japan (537 samples, 20 sites) and the native range in western North America (700 samples, 50 sites). Because chela size is often related to aggressive behavior in crayfish, and hence, their invasion success, we also measured chela size of a subset of specimens in both introduced and native ranges. Genetic diversity of introduced signal crayfish populations was as high as that of the dominant phylogeographic group in the native range, suggesting high propagule pressure during invasion. More recently established crayfish populations in Japan that originated through secondary spread from one of the founding populations exhibit reduced genetic diversity relative to older populations, probably as a result of founder effects. However, these newer populations also show larger chela size, consistent with expectations of rapid adaptations or phenotypic responses during the invasion process. Introduced signal crayfish populations in Japan originate from multiple source populations from a wide geographic range in the native range of western North America. A combination of high genetic diversity, especially for older populations in the invasive range, and rapid adaptation to colonization, manifested as larger chela in recent invasions, likely contribute to invasion success of signal crayfish in Japan.     

A novel approach to parasite population genetics: Experimental infection reveals geographic differentiation,recombination and host‐mediated population structure in Pasteuria ramosa,a bacterial parasite of Daphnia

The population structure of parasites is central to the ecology and evolution of host‐parasite systems. Here, we investigate the population genetics of Pasteuria ramosa, a bacterial parasite of Daphnia. We used natural P. ramosa spore banks from the sediments of two geographically well‐separated ponds to experimentally infect a panel of Daphnia magna host clones whose resistance phenotypes were previously known. In this way, we were able to assess the population structure of P. ramosa based on geography, host resistance phenotype and host genotype. Overall, genetic diversity of P. ramosa was high, and nearly all infected D. magna hosted more than one parasite haplotype. On the basis of the observation of recombinant haplotypes and relatively low levels of linkage disequilibrium, we conclude that P. ramosa engages in substantial recombination. Isolates were strongly differentiated by pond, indicating that gene flow is spatially restricted. Pasteuria ramosa isolates within one pond were segregated completely based on the resistance phenotype of the host—a result that, to our knowledge, has not been previously reported for a nonhuman parasite. To assess the comparability of experimental infections with natural P. ramosa isolates, we examined the population structure of naturally infected D. magna native to one of the two source ponds. We found that experimental and natural infections of the same host resistance phenotype from the same source pond were indistinguishable, indicating that experimental infections provide a means to representatively sample the diversity of P. ramosa while reducing the sampling bias often associated with studies of parasite epidemics. These results expand our knowledge of this model parasite, provide important context for the large existing body of research on this system and will guide the design of future studies of this host‐parasite system.     

Consequences of multiple mating‐system shifts for population and range‐wide genetic structure in a coastal dune plant

Evolutionary transitions from outcrossing to selfing can strongly affect the genetic diversity and structure of species at multiple spatial scales. We investigated the genetic consequences of mating‐system shifts in the North American, Pacific coast dune endemic plant Camissoniopsis cheiranthifolia (Onagraceae) by assaying variation at 13 nuclear (n) and six chloroplast (cp) microsatellite (SSR) loci for 38 populations across the species range. As predicted from the expected reduction in effective population size (N_e) caused by selfing, small‐flowered, predominantly selfing (SF) populations had much lower nSSR diversity (but not cpSSR) than large‐flowered, predominantly outcrossing (LF) populations. The reduction in nSSR diversity was greater than expected from the effects of selfing on N_e alone, but could not be accounted for by indirect effects of selfing on population density. Although selfing should reduce gene flow, SF populations were not more genetically differentiated than LF populations. We detected five clusters of nSSR genotypes and three groups of cpSSR haplotypes across the species range consisting of parapatric groups of populations that usually (but not always) differed in mating system, suggesting that selfing may often initiate ecogeographic isolation. However, lineage‐wide genetic variation was not lower for selfing clusters, failing to support the hypothesis that selection for reproductive assurance spurred the evolution of selfing in this species. Within three populations where LF and SF plants coexist, we detected genetic differentiation among diverged floral phenotypes suggesting that reproductive isolation (probably postzygotic) may help maintain the striking mating‐system differentiation observed across the range of this species.     

A genomic assessment of population structure and gene flow in an aquatic salamander identifies the roles of spatial scale,barriers, and river architecture

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New view of population genetics of zooplankton: RAD‐seq analysis reveals population structure of the North Atlantic planktonic copepod Centropages typicus

Detection of population genetic structure of zooplankton at medium‐to‐small spatial scales in the absence of physical barriers has remained challenging and controversial. The large population sizes and high rates of gene flow characteristic of zooplankton have made resolution of geographical differentiation very difficult, especially when using few genetic markers and assuming equilibrium conditions. Next‐generation sequencing now allows simultaneous sampling of hundreds to thousands of genetic markers; new analytical approaches allow studies under nonequilibrium conditions and directional migration. Samples of the North Atlantic Ocean planktonic copepod, Centropages typicus, were analysed using restriction site‐associated DNA (RAD) sequencing on a PROTON platform. Although prior studies revealed no genetic differentiation of populations across the geographical range of the species, analysis of RAD tags showed significant structure across the North Atlantic Ocean. We also compared the likelihood for models of connectivity among NW Atlantic populations under various directional flow scenarios that replicate oceanographic conditions of the sampled domain. High‐density marker sampling with RAD sequencing markedly outperformed other technical and analytical approaches in detection of population genetic structure and characterization of connectivity of this high geneflow zooplankton species.     

Intercontinental long‐distance seed dispersal across the Mediterranean Basin explains population genetic structure of a bird‐dispersed shrub

Long‐distance dispersal (LDD) is a pivotal process for plants determining their range of distribution and promoting gene flow among distant populations. Most fleshy‐fruited species rely on frugivorous vertebrates to disperse their seeds across the landscape. While LDD events are difficult to record, a few ecological studies have shown that birds move a sizeable number of ingested seeds across geographic barriers, such as sea straits. The foraging movements of migrant frugivores across distant populations, including those separated by geographic barriers, creates a constant flow of propagules that in turn shapes the spatial distributions of the genetic variation in populations. Here, we have analysed the genetic diversity and structure of 74 populations of Pistacia lentiscus, a fleshy‐fruited shrub widely distributed in the Mediterranean Basin, to elucidate whether the Mediterranean Sea acts as a geographic barrier or alternatively whether migratory frugivorous birds promote gene flow among populations located on both sides of the sea. Our results show reduced genetic distances among populations, including intercontinental populations, and they show a significant genetic structure across an eastern‐western axis. These findings are consistent with known bird migratory routes that connect the European and African continents following a north‐southwards direction during the fruiting season of many fleshy‐fruited plants. Further, approximate Bayesian analysis failed to explain the observed patterns as a result of historical population migrations at the end of Last Glacial Maximum. Therefore, anthropic and/or climatic changes that would disrupt the migratory routes of frugivorous birds might have genetic consequences for the plant species they feed upon.     

Patterns of population structure at microsatellite and mitochondrial DNA markers in the franciscana dolphin (Pontoporia blainvillei)

The franciscana dolphin, Pontorporia blainvillei, is an endemic cetacean of the Atlantic coast of South America. Its coastal distribution and restricted movement patterns make this species vulnerable to anthropogenic factors, particularly to incidental bycatch. We used mitochondrial DNA control region sequences, 10 microsatellites, and sex data to investigate the population structure of the franciscana dolphin from a previously established management area, which includes the southern edge of its geographic range. F‐statistics and Bayesian cluster analyses revealed the existence of three genetically distinct populations. Based on the microsatellite loci, similar levels of genetic variability were found in the area; 13 private alleles were found in Monte Hermoso, but none in Claromecó. When considering the mitochondrial DNA control region sequences, lower levels of genetic diversity were found in Monte Hermoso, when compared to the other localities. Low levels of gene flow were found between most localities. Additionally, no evidence of isolation by distance nor sex‐biased dispersal was detected in the study area. In view of these results showing that populations from Necochea/Claromecó, Monte Hermoso, and Río Negro were found to be genetically distinct and the available genetic information for the species previously published, Argentina would comprise five distinct populations: Samborombón West/Samborombón South, Cabo San Antonio/Buenos Aires East, Necochea/Claromecó/Buenos Aires Southwest, Monte Hermoso, and Río Negro. In order to ensure the long‐term survival of the franciscana dolphin, management and conservation strategies should be developed considering each of these populations as different management units.     

Black rat invasion of inland Sahel: insights from interviews and population genetics in south‐western Niger

Human population migrations, as well as long‐distance trade activities, have been responsible for the spread of many invasive organisms. The black rat, Rattus rattus, has colonized most of the world following ship‐mediated trade. Owing to its tight association with human infrastructures, this species has been able to survive in unfavourable environments, such as Sahelian Africa. In this work, we combined interview‐based and population genetic surveys to investigate the processes underlying the ongoing invasion of south‐western Niger by black rats, with special emphasis on the capital city, Niamey. Our trapping and interview data are quite congruent, and all together point towards a patchy, but rather widespread, current distribution of R. rattus. Genetic data strongly suggest that road network development for truck‐based commercial flow from/to international harbours located in neighbouring countries (Benin, Togo, and Nigeria) facilitates the passive dispersal of black rats over a long distance through unfavourable landscapes. Another potentially, more ancient, invasion route may be associated with boat transport along the Niger River. Human‐mediated dispersal thus probably allows the foundation of persisting populations within highly anthropized areas while population dynamics may be more unstable in remote areas and mostly depends on propagule pressure.