Population structure and dispersal of the coral‐excavating sponge Cliona delitrix

Some excavating sponges of the genus Cliona compete with live reef corals, often killing and bioeroding entire colonies. Important aspects affecting distribution of these species, such as dispersal capability and population structure, remain largely unknown. Thus, the aim of this study was to determine levels of genetic connectivity and dispersal of Cliona delitrix across the Greater Caribbean (Caribbean Sea, Bahamas and Florida), to understand current patterns and possible future trends in their distribution and effects on coral reefs. Using ten species‐specific microsatellite markers, we found high levels of genetic differentiation between six genetically distinct populations: one in the Atlantic (Florida‐Bahamas), one specific to Florida and four in the South Caribbean Sea. In Florida, two independent breeding populations are likely separated by depth. Gene flow and ecological dispersal occur among other populations in the Florida reef tract, and between some Florida locations and the Bahamas. Similarly, gene flow occurs between populations in the South Caribbean Sea, but appears restricted between the Caribbean Sea and the Atlantic (Florida‐Bahamas). Dispersal of C. delitrix was farther than expected for a marine sponge and favoured in areas where currents are strong enough to transport sponge eggs or larvae over longer distances. Our results support the influence of ocean current patterns on genetic connectivity, and constitute a baseline to monitor future C. delitrix trends under climate change.     

Geography,seasonality, and host‐associated population structure influence the fecal microbiome of a genetically depauparate Arctic mammal

The Canadian Arctic is an extreme environment with low floral and faunal diversity characterized by major seasonal shifts in temperature, moisture, and daylight. Muskoxen (Ovibos moschatus) are one of few large herbivores able to survive this harsh environment. Microbiome research of the gastrointestinal tract may hold clues as to how muskoxen exist in the Arctic, but also how this species may respond to rapid environmental changes. In this study, we investigated the effects of season (spring/summer/winter), year (2007–2016), and host genetic structure on population‐level microbiome variation in muskoxen from the Canadian Arctic. We utilized 16S rRNA gene sequencing to characterize the fecal microbial communities of 78 male muskoxen encompassing two population genetic clusters. These clusters are defined by Arctic Mainland and Island populations, including the following: (a) two mainland sampling locations of the Northwest Territories and Nunavut and (b) four locations of Victoria Island. Between these geographic populations, we found that differences in the microbiome reflected host‐associated genetic cluster with evidence of migration. Within populations, seasonality influenced bacterial diversity with no significant differences between years of sampling. We found evidence of pathogenic bacteria, with significantly higher presence in mainland samples. Our findings demonstrate the effects of seasonality and the role of host population‐level structure in driving fecal microbiome differences in a large Arctic mammal.     

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.     

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.     

Self‐fertilization,long‐distance flash invasion and biogeography shape the population structure of Pseudosuccinea columella at the worldwide scale

Population genetic studies are efficient for inferring the invasion history based on a comparison of native and invasive populations, especially when conducted at species scale. An expected outcome in invasive populations is variability loss, and this is especially true in self‐fertilizing species. We here focus on the self‐fertilizing Pseudosuccinea columella, an invasive hermaphroditic freshwater snail that has greatly expanded its geographic distribution and that acts as intermediate host of Fasciola hepatica, the causative agent of human and veterinary fasciolosis. We evaluated the distribution of genetic diversity at the largest geographic scale analysed to date in this species by surveying 80 populations collected during 16 years from 14 countries, using eight nuclear microsatellites and two mitochondrial genes. As expected, populations from North America, the putative origin area, were strongly structured by selfing and history and harboured much more genetic variability than invasive populations. We found high selfing rates (when it was possible to infer it), none‐to‐low genetic variability and strong population structure in most invasive populations. Strikingly, we found a unique genotype/haplotype in populations from eight invaded regions sampled all over the world. Moreover, snail populations resistant to infection by the parasite are genetically distinct from susceptible populations. Our results are compatible with repeated introductions in South America and flash worldwide invasion by this unique genotype/haplotype. Our study illustrates the population genetic consequences of biological invasion in a highly selfing species at very large geographic scale. We discuss how such a large‐scale flash invasion may affect the spread of fasciolosis.     

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.     

Urban population genetics of slum‐dwelling rats (Rattus norvegicus) in Salvador,Brazil

Throughout the developing world, urban centres with sprawling slum settlements are rapidly expanding and invading previously forested ecosystems. Slum communities are characterized by untended refuse, open sewers and overgrown vegetation, which promote rodent infestation. Norway rats (Rattus norvegicus) are reservoirs for epidemic transmission of many zoonotic pathogens of public health importance. Understanding the population ecology of R. norvegicus is essential to formulate effective rodent control strategies, as this knowledge aids estimation of the temporal stability and spatial connectivity of populations. We screened for genetic variation, characterized the population genetic structure and evaluated the extent and patterns of gene flow in the urban landscape using 17 microsatellite loci in 146 rats from nine sites in the city of Salvador, Brazil. These sites were divided between three neighbourhoods within the city spaced an average of 2.7 km apart. Surprisingly, we detected very little relatedness among animals trapped at the same site and found high levels of genetic diversity, as well as structuring across small geographical distances. Most F_ST comparisons among sites were statistically significant, including sites <400 m apart. Bayesian analyses grouped the samples in three genetic clusters, each associated with distinct sampling sites from different neighbourhoods or valleys within neighbourhoods. These data indicate the existence of complex genetic structure in R. norvegicus in Salvador, linked to the heterogeneous urban landscape. Future rodent control measures need to take into account the spatial and temporal linkage of rat populations in Salvador, as revealed by genetic data, to develop informed eradication strategies.     

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.     

Phylogeography and population genetics of pine butterflies: Sky islands increase genetic divergence

The sky islands of southeastern Arizona (AZ) mark a major transition zone between tropical and temperate biota and are considered a neglected biodiversity hotspot. Dispersal ability and host plant specificity are thought to impact the history and diversity of insect populations across the sky islands. We aimed to investigate the population structure and phylogeography of two pine‐feeding pierid butterflies, the pine white (Neophasia menapia) and the Mexican pine white (Neophasia terlooii), restricted to these “islands” at this transition zone. Given their dependence on pines as the larval hosts, we hypothesized that habitat connectivity affects population structure and is at least in part responsible for their allopatry. We sampled DNA from freshly collected butterflies from 17 sites in the sky islands and adjacent high‐elevation habitats and sequenced these samples using ddRADSeq. Up to 15,399 SNPs were discovered and analyzed in population genetic and phylogenetic contexts with Stacks and pyRAD pipelines. Low genetic differentiation in N. menapia suggests that it is panmictic. Conversely, there is strong evidence for population structure within N. terlooii. Each sky island likely contains a population of N. terlooii, and clustering is hierarchical, with populations on proximal mountains being more related to each other. The N. menapia habitat, which is largely contiguous, facilitates panmixia, while the N. terlooii habitat, restricted to the higher elevations on each sky island, creates distinct population structure. Phylogenetic results corroborate those from population genetic analyses. The historical climate‐driven fluxes in forest habitat connectivity have implications for understanding the biodiversity of fragmented habitats.     

Spatial structuring of the population genetics of a European subterranean termite species

In population genetics studies, detecting and quantifying the distribution of genetic variation can help elucidate ecological and evolutionary processes. In social insects, the distribution of population‐level genetic variability is generally linked to colony‐level genetic structure. It is thus especially crucial to conduct complementary analyses on such organisms to examine how spatial and social constraints interact to shape patterns of intraspecific diversity. In this study, we sequenced the mitochondrial COII gene for 52 colonies of the subterranean termite Reticulitermes grassei (Isoptera: Rhinotermitidae), sampled from a population in southwestern France. Three haplotypes were detected, one of which was found exclusively in the southern part of the study area (near the Pyrenees). After genotyping 6 microsatellite loci for 512 individual termites, we detected a significant degree of isolation by distance among individuals over the entire range; however, the cline of genetic differentiation was not continuous, suggesting the existence of differentiated populations. A spatial principal component analysis based on allele frequency data revealed significant spatial autocorrelation among genotypes: the northern and southern groups were strongly differentiated. This finding was corroborated by clustering analyses; depending on the randomized data set, two or three clusters, exhibiting significant degrees of differentiation, were identified. An examination of colony breeding systems showed that colonies containing related neotenic reproductives were prevalent, suggesting that inbreeding may contribute to the high level of homozygosity observed and thus enhance genetic contrasts among colonies. We discuss the effect of evolutionary and environmental factors as well as reproductive and dispersal modes on population genetic structure.     

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.     

Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program structure

Reproducibility is the benchmark for results and conclusions drawn from scientific studies, but systematic studies on the reproducibility of scientific results are surprisingly rare. Moreover, many modern statistical methods make use of ‘random walk’ model fitting procedures, and these are inherently stochastic in their output. Does the combination of these statistical procedures and current standards of data archiving and method reporting permit the reproduction of the authors' results? To test this, we reanalysed data sets gathered from papers using the software package structure to identify genetically similar clusters of individuals. We find that reproducing structure results can be difficult despite the straightforward requirements of the program. Our results indicate that 30% of analyses were unable to reproduce the same number of population clusters. To improve this, we make recommendations for future use of the software and for reporting structure analyses and results in published works.     

Sunshine versus gold: The effect of population age on genetic structure of an invasive mosquito

The genetic diversity and structure of invasive species are affected by the time since invasion, but it is not well understood how. We compare likely the oldest populations of Aedes aegypti in continental North America with some of the newest to illuminate the range of genetic diversity and structure that can be found within the invasive range of this important disease vector. Aedes aegypti populations in Florida have probably persisted since the 1600‐1700s, while populations in southern California derive from new invasions that occurred in the last 10 years. For this comparison, we genotyped 1,193 individuals from 28 sites at 12 highly variable microsatellites and a subset of these individuals at 23,961 single nucleotide polymorphisms (SNPs). This is the largest sample analyzed for genetic structure for either region, and it doubles the number of southern California populations previously analyzed. As predicted, the older populations (Florida) showed fewer indicators of recent founder effect and bottlenecks; in particular, these populations have dramatically higher genetic diversity and lower genetic structure. Geographic distance and driving distance were not good predictors of genetic distance in either region, especially southern California. Additionally, southern California had higher levels of genetic differentiation than any comparably sized documented region throughout the worldwide distribution of the species. Although population age and demographic history are likely driving these differences, differences in climate and transportation practices could also play a role.     

Effects of eutrophication on bioeroding sponge communities with the description of new West Indian sponges, Cliona spp. (Porifera: Hadromerida: Clionidae)

Abstract. Pieces of coral rubble ( Porites porites ), collected from across 3 fringing reefs that lie along a eutrophication gradient, were examined for the presence of clionid sponges. A similarity analysis of species composition showed that reef zone had less effect on clionid community composition than did other factors affecting the reefs as a whole. Except on the back reef, the Zones, distances, and depths within the reefs had no significant influence on the number of clionid invasions. Reef comparisons demonstrated that clionid abundance increased with increasing eutrophication. Clionids were found in 41% of the pieces collected from the most eutrophic site vs. 24% from the least eutrophic. Because clionids are the principal bio-eroders of coral reefs, any increase in their abundance will likely result in greater bioerosion rates. The mean abundance of Type 3 corals (in which fragmentation is the primary mode of propagation) is positively related to the frequency of boring sponge invasion. suggesting that increased bioerosion may be partly responsible for community shifts toward Type 3 corals in polluted waters. Cliona cf. vastifica , found for the first time in Barbados, flourishes on the most eutrophic reef and may become an important bioeroder under the highly eutrophic conditions that have begun to plague West Indian reefs. Two new species of Cliona (Porifera: Hadro-merida: Clionidae) are described.     

Symbiodinium population genetics: testing for species boundaries and analysing samples with mixed genotypes

Population genetic markers are increasingly being used to study the diversity, ecology and evolution of Symbiodinium, a group of eukaryotic microbes that are often mutualistic with reef‐building corals. Population genetic markers can resolve individual clones, or strains, from samples of host tissue; however, samples may comprise different species that may confound interpretations of gene flow and genetic structure. Here, we propose a method for resolving species from population genetic data using tests for genetic recombination. Assigning individuals to genetically recombining populations prior to further analyses avoids critical errors in the interpretation of gene flow and dispersal. To demonstrate the effectiveness of the approach, we first apply this method to a simulated data set. We then use the method to resolve two species of host generalist Symbiodinium that commonly co‐occur in reef‐building corals collected from Indo‐West Pacific reefs. We demonstrate that the method is robust even when some hosts contain genotypes from two distinct species. Finally, we examine population genetic data sets from two recently published papers in Molecular Ecology. We show that each strongly supports a two species interpretation, which significantly changes the original conclusions presented in these studies. When combined with available phylogenetic and ecological evidence, the use of population genetic data offers a robust method for unambiguously delimiting morphologically cryptic species.     

Host behaviour drives parasite genetics at multiple geographic scales: population genetics of the chewing louse,Thomomydoecus minor

Pocket gophers and their symbiotic chewing lice form a host–parasite assemblage known for a high degree of cophylogeny, thought to be driven by life history parameters of both host and parasite that make host switching difficult. However, little work to date has focused on determining whether these life histories actually impact louse populations at the very fine scale of louse infrapopulations (individuals on a single host) at the same or at nearby host localities. We used microsatellite and mtDNA sequence data to make comparisons of chewing‐louse (Thomomydoecus minor) population subdivision over time and over geographic space where there are different potential amounts of host interaction surrounding a zone of contact between two hybridizing pocket‐gopher subspecies. We found that chewing lice had high levels of population isolation consistent with a paucity of horizontal transmission even at the very fine geographic scale of a single alfalfa field. We also found marked genetic discontinuity in louse populations corresponding with host subspecies and little, if any, admixture in the louse genetic groups even though the lice are closely related. The correlation of louse infrapopulation differentiation with host interaction at multiple scales, including across a discontinuity in pocket‐gopher habitat, suggests that host behaviour is the primary driver of parasite genetics. This observation makes sense in light of the life histories of both chewing lice and pocket gophers and provides a powerful explanation for the well‐documented pattern of parallel cladogenesis in pocket gophers and chewing lice.     

Host specificity shapes population structure of pinworm parasites in Caribbean reptiles

Host specificity is one of the potential factors affecting parasite diversification because gene flow may be facilitated or constrained by the number of host species that a parasite can exploit. We test this hypothesis using a costructure approach, comparing two sympatric pinworm parasites that differ in host specificity – Parapharyngodon cubensis and Spauligodon anolis – on the Puerto Rican Bank and St. Croix in the Caribbean. Spauligodon anolis specializes on Anolis lizards, whereas P. cubensis parasitizes Anolis lizards as well as many other species of lizards and snakes. We collected lizards from across the Puerto Rican Bank and St. Croix, sampled them for S. anolis and P. cubensis and generated nuclear and mitochondrial sequence data from the parasites. We used these data to show that P. cubensis is comprised of multiple cryptic species that exhibit limited population structure relative to S. anolis, which is consistent with our prediction based on their host specificity. We also provide evidence that the distribution of P. cubensis species is maintained by competitive exclusion, and in contrast to previous theoretical work, the parasites with the greatest number of host species also reach the highest prevalence rates. Overall, our results are consistent with the hypothesis that host specificity shapes parasite diversification, and suggest that even moderate differences in host specificity may contribute to substantial differences in diversification.     

Population genetics of the people of Iran II. Genetic differentiation and population structure

The genetic structure of six populations of Iran (Turks, Kurds, Lurs, Zabolis, Baluchis and Zoroastrians) was examined using data on blood groups, serum proteins and cell enzymes. Our results show conclusively that there are genetic differences among the six populations and the analysis of superimposed R and S matrices defined Harpending & Jenkins (1973) show by that the dispersion of some of the alleles correspond to the dispersion of the populations. The F_ST estimates are not large enough to favour selection on any of the loci studied. The F_IT and F_IS estimates are positive and moderately high suggesting that the genetic differentiation to some extent is influenced by inbreeding.