Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline

This study presents genetic evidence that whale sharks, Rhincodon typus, are comprised of at least two populations that rarely mix and is the first to document a population expansion. Relatively high genetic structure is found when comparing sharks from the Gulf of Mexico with sharks from the Indo‐Pacific. If mixing occurs between the Indian and Atlantic Oceans, it is not sufficient to counter genetic drift. This suggests whale sharks are not all part of a single global metapopulation. The significant population expansion we found was indicated by both microsatellite and mitochondrial DNA. The expansion may have happened during the Holocene, when tropical species could expand their range due to sea‐level rise, eliminating dispersal barriers and increasing plankton productivity. However, the historic trend of population increase may have reversed recently. Declines in genetic diversity are found for 6 consecutive years at Ningaloo Reef in Australia. The declines in genetic diversity being seen now in Australia may be due to commercial‐scale harvesting of whale sharks and collision with boats in past decades in other countries in the Indo‐Pacific. The study findings have implications for models of population connectivity for whale sharks and advocate for continued focus on effective protection of the world's largest fish at multiple spatial scales.     

Isolation and genetic diversity of endangered grey nurse shark (Carcharias taurus) populations

Anthropogenic impacts are believed to be the primary threats to the eastern Australian population of grey nurse sharks (Carcharias taurus), which is listed as critically endangered, and the most threatened population globally. Analyses of 235 polymorphic amplified fragment length polymorphisms (AFLP) loci and 700 base pairs of mitochondrial DNA control region provide the first account of genetic variation and geographical partitioning (east and west coasts of Australia, South Africa) in C. taurus. Assignment tests, analysis of relatedness and Fst values all indicate that the Australian populations are isolated from South Africa, with negligible migration between the east and west Australian coasts. There are significant differences in levels of genetic variation among regions. Australian C. taurus, particularly the eastern population, has significantly less AFLP variation than the other sampling localities. Further, the eastern Australian sharks possess only a single mitochondrial haplotype, also suggesting a small number of founding individuals. Therefore, historical, rather than anthropogenic processes most likely account for their depauperate genetic variation. These findings have implications for the viability of the eastern Australian population of grey nurse sharks.     

Relatedness and polyandry of sixgill sharks, <Emphasis Type="Italic">Hexanchus griseus</Emphasis>, in an urban estuary

The bluntnose sixgill shark (Hexanchus griseus) is a widely distributed species found in tropical and temperate waters of every ocean, yet we know relatively little about their basic biology including their life history and population structure. From 2003–2007, we collected over 300 biopsy samples from sixgills during research operations in Puget Sound, WA, USA. Genotypic data using ten polymorphic microsatellites were used to describe sixgill genetic diversity, relatedness and mating pattern. Diversity within sixgills was found to be moderate with an average observed heterozygosity of 0.45, an average expected heterozygosity of 0.61, an average of 12 alleles per locus, and an average allelic richness of eight within microsatellite loci. Our data suggests all of the sampled individuals come from one intermixing population, and we found no historical evidence of significant population bottlenecks. Many of the sharks were sampled using longline techniques with several sharks captured at the same time and place. Similarly, multiple sharks were sampled on several occasions during research events at the Seattle Aquarium. The proportion of individuals that were full- or half-siblings was high among sharks sampled at the same time and place (range 0.65–0.87). Analysis of the genetic relationship between one large female washed ashore and 71 of her near-term pups suggested a polyandrous mating system with as many as nine males contributing to her offspring. This study is the first to investigate genetic diversity, relatedness and paternity within sixgill sharks and sheds light on important conservation implications for this little known shark population.     

Microsatellite Analyses of Blacktip Reef Sharks (Carcharhinus melanopterus) in a Fragmented Environment Show Structured Clusters

The population dynamics of shark species are generally poorly described because highly mobile marine life is challenging to investigate. Here we investigate the genetic population structure of the blacktip reef shark (Carcharhinus melanopterus) in French Polynesia. Five demes were sampled from five islands with different inter-island distances (50–1500 km). Whether dispersal occurs between islands frequently enough to prevent moderate genetic structure is unknown. We used 11 microsatellites loci from 165 individuals and a strong genetic structure was found among demes with both F-statistics and Bayesian approaches. This differentiation is correlated with the geographic distance between islands. It is likely that the genetic structure seen is the result of all or some combination of the following: low gene flow, time since divergence, small effective population sizes, and the standard issues with the extent to which mutation models actually fit reality. We suggest low levels of gene flow as at least a partial explanation of the level of genetic structure seen among the sampled blacktip demes. This explanation is consistent with the ecological traits of blacktip reef sharks, and that the suitable habitat for blacktips in French Polynesia is highly fragmented. Evidence for spatial genetic structure of the blacktip demes we studied highlights that similar species may have populations with as yet undetected or underestimated structure. Shark biology and the market for their fins make them highly vulnerable and many species are in rapid decline. Our results add weight to the case that total bans on shark fishing are a better conservation approach for sharks than marine protected area networks.     

Genetic consequences of trumpeter swan (Cygnus buccinator) reintroductions

Relocation programs are often initiated to restore threatened species to previously occupied portions of their range. A primary challenge of restoration efforts is to translocate individuals in a way that prevents loss of genetic diversity and decreases differentiation relative to source populations—a challenge that becomes increasingly difficult when remnant populations of the species are already genetically depauperate. Trumpeter swans were previously extirpated in the entire eastern half of their range. Physical translocations of birds over the last 70 years have restored the species to portions of its historical range. Despite the long history of management, there has been little monitoring of the genetic outcomes of these restoration attempts. We assessed the consequences of this reintroduction program by comparing patterns of genetic variation at 17 microsatellite loci across four restoration flocks (three wild-released, one captive) and their source populations. We found that a wild-released population established from a single source displayed a trend toward reduced genetic diversity relative to and significant genetic differentiation from its source population, though small founder population effects may also explain this pattern. Wild-released flocks restored from multiple populations maintained source levels of genetic variation and lacked significant differentiation from at least one of their sources. Further, the flock originating from a single source revealed significantly lower levels of genetic variation than those established from multiple sources. The distribution of genetic variation in the captive flock was similar to its source. While the case of trumpeter swans provides evidence that restorations from multiple versus single source populations may better preserve natural levels of genetic diversity, more studies are needed to understand the general applicability of this management strategy.     

Low genetic diversity and high genetic divergence caused by inbreeding and geographical isolation in the populations of endangered species Loropetalum subcordatum (Hamamelidaceae) endemic to China

Loropetalum subcordatum (Hamamelidaceae) is one of the most endangered angiosperm species in China. It is narrowly distributed in a few localities in the evergreen broadleaved forest of southern China. Up to now only a few dozen remnant individuals have been found in the four extant populations. In this project, we studied its genetic diversity and population genetic structure using the high resolution molecular marker of amplified fragment length polymorphism. In total, 47 individuals from all the four populations (including all individuals in three populations) were analyzed. Comparably low genetic diversity within populations was revealed and significantly high genetic differentiation among the populations was detected. Four independent groups were identified which corresponded with their geographical ranges. Autogamy is considered to be the major factor contributing to the low genetic variation and high genetic divergence within this species. In addition, small population size, restricted distribution range, geographical isolation and limited seed dispersal may also contribute to the low genetic diversity and high population genetic differentiation. Clonal reproduction was inferred to occur in the two island populations. Suggestions for conservation strategies are provided to preserve the genetic resources of this species.     

Are indirect genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks

Multiple mating has clear fitness benefits for males, but uncertain benefits and costs for females. We tested for indirect genetic benefits of polyandry in a natural population, by using data from a long-term genetic and demographic study of lemon sharks ( Negaprion brevirostris ) at Bimini, Bahamas. To do so, we followed the fates of individuals from six cohorts (450 age-0 and 254 age-1 fish) in relation to their individual level of genetic variation, and whether they were from polyandrous or monoandrous litters. We find that offspring from polyandrous litters did not have a greater genetic diversity or greater survival than did the offspring of monoandrous litters. We also find no evidence of positive associations between individual offspring genetic diversity metrics and our surrogate measure of fitness (i.e. survival). In fact, age-1 individuals with fewer heterozygous microsatellite loci and more genetically similar parents were more likely to survive to age-2. Thus, polyandry in female lemon sharks does not appear to be adaptive from the perspective of indirect genetic benefits to offspring. It may instead be the result of convenience polyandry, whereby females mate multiply to avoid harassment by males. Our inability to find indirect genetic benefits of polyandry despite detailed pedigree and survival information suggests the need for similar assessments in other natural populations.     

Genetic rescue in a severely inbred wolf population

Natural populations are becoming increasingly fragmented which is expected to affect their viability due to inbreeding depression, reduced genetic diversity and increased sensitivity to demographic and environmental stochasticity. In small and highly inbred populations, the introduction of only a few immigrants may increase vital rates significantly. However, very few studies have quantified the long‐term success of immigrants and inbred individuals in natural populations. Following an episode of natural immigration to the isolated, severely inbred Scandinavian wolf (Canis lupus) population, we demonstrate significantly higher pairing and breeding success for offspring to immigrants compared to offspring from native, inbred pairs. We argue that inbreeding depression is the underlying mechanism for the profound difference in breeding success. Highly inbred wolves may have lower survival during natal dispersal as well as competitive disadvantage to find a partner. Our study is one of the first to quantify and compare the reproductive success of first‐generation offspring from migrants vs. native, inbred individuals in a natural population. Indeed, our data demonstrate the profound impact single immigrants can have in small, inbred populations, and represent one of very few documented cases of genetic rescue in a population of large carnivores.     

Extremely low genetic diversity and extensive genetic admixture at the northern range margins of Bombax ceiba

Understanding the evolutionary processes in species at the margins of their range is of great significance, because marginal populations may harbor local adaptations and will initiate further expansion in response to changes in the environment. Here we examined genetic variation in two nuclear genes and one chloroplast intergenic spacer in 13 northern marginal populations and one geographically central population of Bombax ceiba, a tree distributed mainly in tropical regions. Our results revealed an extremely low level of genetic diversity in each population at the northern margin of its range and strong genetic differentiation between southern China and South Asia. Cultivated and natural populations showed no significant differences in genetic variability. Genetic admixture in a nuclear gene was detected in 10 of the 13 populations at the northern margin of their range. The founder effect, in which a small number of individuals colonize the northern margins of its range, may explain the extremely low genetic diversity. During the establishment of new populations, different source populations may mix and undergo further genetic drift and differentiation. This study indicates that patterns of genetic diversity in tropical species at the margin of their range may also be severely influenced by founder effects.     

Movement Patterns of Juvenile Whale Sharks Tagged at an Aggregation Site in the Red Sea

Conservation efforts aimed at the whale shark, Rhincodon typus, remain limited by a lack of basic information on most aspects of its ecology, including global population structure, population sizes and movement patterns. Here we report on the movements of 47 Red Sea whale sharks fitted with three types of satellite transmitting tags from 2009–2011. Most of these sharks were tagged at a single aggregation site near Al-Lith, on the central coast of the Saudi Arabian Red Sea. Individuals encountered at this site were all juveniles based on size estimates ranging from 2.5–7 m total length with a sex ratio of approximately 1∶1. All other known aggregation sites for juvenile whale sharks are dominated by males. Results from tagging efforts showed that most individuals remained in the southern Red Sea and that some sharks returned to the same location in subsequent years. Diving data were recorded by 37 tags, revealing frequent deep dives to at least 500 m and as deep as 1360 m. The unique temperature-depth profiles of the Red Sea confirmed that several whale sharks moved out of the Red Sea while tagged. The wide-ranging horizontal movements of these individuals highlight the need for multinational, cooperative efforts to conserve R. typus populations in the Red Sea and Indian Ocean.     

World without borders—genetic population structure of a highly migratory marine predator,the blue shark (Prionace glauca)

Highly migratory, cosmopolitan oceanic sharks often exhibit complex movement patterns influenced by ontogeny, reproduction, and feeding. These elusive species are particularly challenging to population genetic studies, as representative samples suitable for inferring genetic structure are difficult to obtain. Our study provides insights into the genetic population structure one of the most abundant and wide‐ranging oceanic shark species, the blue shark Prionace glauca, by sampling the least mobile component of the populations, i.e., young‐of‐year and small juveniles (<2 year; N = 348 individuals), at three reported nursery areas, namely, western Iberia, Azores, and South Africa. Samples were collected in two different time periods (2002–2008 and 2012–2015) and were screened at 12 nuclear microsatellites and at a 899‐bp fragment of the mitochondrial control region. Our results show temporally stable genetic homogeneity among the three Atlantic nurseries at both nuclear and mitochondrial markers, suggesting basin‐wide panmixia. In addition, comparison of mtDNA CR sequences from Atlantic and Indo‐Pacific locations also indicated genetic homogeneity and unrestricted female‐mediated gene flow between ocean basins. These results are discussed in light of the species' life history and ecology, but suggest that blue shark populations may be connected by gene flow at the global scale. The implications of the present findings to the management of this important fisheries resource are also discussed.     

Phylogeography and conservation of the bull shark (Carcharhinus leucas) inferred from mitochondrial and microsatellite DNA

The bull shark (Carcharhinus leucas) is a widely distributed, large coastal shark species known to travel long distances. These characteristics, coupled with the species?? long life span and late age of maturity, would lead one to predict significant global genetic exchange among bull shark populations. By contrast, data show localized depletion in some areas of large coastal shark fisheries, indicating some geographic isolation may exist. We examined genetic variation in the control region of mitochondrial DNA and at five nuclear microsatellite loci in bull sharks sampled from the western Atlantic to investigate the degree of population subdivision. The average per sample haplotype and nucleotide diversity in the mtDNA (0.51 ± 0.26 and 0.12% ± 0.12, respectively) and expected heterozygosity (0.84) in the microsatellite loci contrast sharply in having lower and higher values (respectively) relative to many other shark species. Significant structure exists between the Brazilian and all northern populations at the mtDNA control region (pairwise ??_ST > 0.8, P < 0.001), but not at the nuclear microsatellite loci. Adjacent northern populations show weak to no genetic differentiation for both markers. These results are congruent with restricted maternal gene flow between populations caused by female site fidelity to nursery areas. We estimate the current effective population size to be around 160,000 and 221,000 individuals for the southern and northern Atlantic populations, respectively. The philopatric habits and the relatively low levels of mtDNA genetic diversity observed in bull sharks must be considered in the conservation of this species. Our results indicate that effective bull shark management strategies will require local, regional, and international attention and cooperation.     

Population genetic structure of Earth's largest fish, the whale shark (Rhincodon typus)

Large pelagic vertebrates pose special conservation challenges because their movements generally exceed the boundaries of any single jurisdiction. To assess the population structure of whale sharks (Rhincodon typus), we sequenced complete mitochondrial DNA control regions from individuals collected across a global distribution. We observed 51 single site polymorphisms and 8 regions with indels comprising 44 haplotypes in 70 individuals, with high haplotype (h = 0.974 +/- 0.008) and nucleotide diversity (pi = 0.011 +/- 0.006). The control region has the largest length variation yet reported for an elasmobranch (1143-1332 bp). Phylogenetic analyses reveal no geographical clustering of lineages and the most common haplotype was distributed globally. The absence of population structure across the Indian and Pacific basins indicates that oceanic expanses and land barriers in Southeast Asia are not impediments to whale shark dispersal. We did, however, find significant haplotype frequency differences (AMOVA, Phi(ST) = 0.107, P < 0.001) principally between the Atlantic and Indo-Pacific populations. In contrast to other recent surveys of globally distributed sharks, we find much less population subdivision and no evidence for cryptic evolutionary partitions. Discovery of the mating and pupping areas of whale sharks is key to further population genetic studies. The global pattern of shared haplotypes in whale sharks provides a compelling argument for development of broad international approaches for management and conservation of Earth's largest fish.     

Genetic vulnerability of a remnant ant population

Ants are ecologically important species in many environments forming a big proportion of the total animal biomass. However, their special features such as sociality and complementary sex-determination system have received little attention in conservation discussions. We examined the social and genetic structure of the hairy wood ant Formica lugubris in Ireland to evaluate factors relevant to the vulnerability of small, isolated wood ant populations. We also clarified the conservation status of the species in Ireland. Our results showed that the populations are mainly monogynous (one queen per nest). Consequently the effective population size is very low (<100 individuals) in Ireland. We found extremely little genetic variation, signs of inbreeding and inbreeding depression, which can be a consequence of the small effective population size and of the restricted gene flow due to strong isolation of populations. Putatively high genetic diversity at the sex-determining locus can reflect a larger population in the past. The study shows that even though the population may seem stable because of the long life span of queen ants, sociality can impact species conservation by keeping the effective population size small. According to our results, the hairy wood ant can be considered native to Ireland. Hence it needs urgent protection and the genetic issues need to be considered in the future management strategies.     

Temporal trends in genetic data and effective population size support efficacy of management practices in critically endangered dusky gopher frogs (Lithobates sevosus)

Monitoring temporal changes in population genetic diversity and effective population size can provide vital information on future viability. The dusky gopher frog, Lithobates sevosus, is a critically endangered species found only in coastal Mississippi, with low genetic variability as a consequence of isolation and population size reduction. Conservation management practices have been implemented, but their efficacy has not been addressed. We genotyped individuals collected 1997–2014 to determine temporal trends in population genetic variation, structure, and effective size. Observed and expected heterozygosity and allelic richness revealed temporally stable, but low, levels of genetic variation. Positive levels of inbreeding were found in each year. There was weak genetic structure among years, which can be attributed to increased effects of genetic drift and inbreeding in small populations. L. sevosus exhibited an increase in effective population size, and currently has an estimated effective size of 33.0–58.6 individuals, which is approximately half the census size. This large ratio could possibly be explained by genetic compensation. We found that management practices have been effective at maintaining and improving effective size and genetic diversity, but that additional strategies need to be implemented to enhance viability of the species.     

Unexpected heterozygosity in an island mouflon population founded by a single pair of individuals

In population and conservation genetics, there is an overwhelming body of evidence that genetic diversity is lost over time in small populations. This idea has been supported by comparative studies showing that small populations have lower diversity than large populations. However, longitudinal studies reporting a decline in genetic diversity throughout the whole history of a given wild population are much less common. Here, we analysed changes in heterozygosity over time in an insular mouflon (Ovis aries) population founded by two individuals in 1957 and located on one of the most isolated locations in the world: the Kerguelen Sub-Antarctic archipelago. Heterozygosity measured using 25 microsatellite markers has actually increased over 46 years since the introduction, and exceeds the range predicted by neutral genetic models and stochastic simulations. Given the complete isolation of the population and the short period of time since the introduction, changes in genetic variation cannot be attributed to mutation or migration. Several lines of evidence suggest that the increase in heterozygosity with time may be attributable to selection. This study shows the importance of longitudinal genetic surveys for understanding the mechanisms that regulate genetic diversity in wild populations.     

Native American Admixture in the Quebec Founder Population

For years, studies of founder populations and genetic isolates represented the mainstream of genetic mapping in the effort to target genetic defects causing Mendelian disorders. The genetic homogeneity of such populations as well as relatively homogeneous environmental exposures were also seen as primary advantages in studies of genetic susceptibility loci that underlie complex diseases. European colonization of the St-Lawrence Valley by a small number of settlers, mainly from France, resulted in a founder effect reflected by the appearance of a number of population-specific disease-causing mutations in Quebec. The purported genetic homogeneity of this population was recently challenged by genealogical and genetic analyses. We studied one of the contributing factors to genetic heterogeneity, early Native American admixture that was never investigated in this population before. Consistent admixture estimates, in the order of one per cent, were obtained from genome-wide autosomal data using the ADMIXTURE and HAPMIX software, as well as with the fastIBD software evaluating the degree of the identity-by-descent between Quebec individuals and Native American populations. These genomic results correlated well with the genealogical estimates. Correlations are imperfect most likely because of incomplete records of Native founders’ origin in genealogical data. Although the overall degree of admixture is modest, it contributed to the enrichment of the population diversity and to its demographic stratification. Because admixture greatly varies among regions of Quebec and among individuals, it could have significantly affected the homogeneity of the population, which is of importance in mapping studies, especially when rare genetic susceptibility variants are in play.     

普通野生稻小种群的交配系统与遗传多样性

小种群的遗传动态是保育遗传学关注的核心问题之一,而种群遗传动态又与交配系统密切相关.普通野生稻(Oryza rufipogon Griff.)是具有重要经济价值的濒危物种,目前其种群规模都较小,研究其小种群交配系统与遗传变异性对普通野生稻的保护具有重要意义.运用7对SSR引物,对采自江西东乡普通野生稻小种群的36份种茎和其中20个家系共计601份子代进行了分析.结果显示:该种群的表观异交率为0.318,多位点法估计(MLTR)的多位点异交率为0.481;50%以上的子代共享亲本,非随机交配明显;东乡普通野生稻种群交配系统属于混合交配类型.比较亲本和子代种群的遗传变异性显示:子代种群比亲本种群遗传变异性更丰富;子代种群的杂合子不足与种群变小自交比例上升有关;而亲本种群杂合子过剩可能与杂合基因型的选择优势有关.这些结果说明创造条件扩大种群规模对普通野生稻的原生境保护显得尤为重要.     

Conservation Genetics of Jacquemontia reclinata (Convolvulaceae), an Endangered Species from Southern Florida: Implications for Restoration Management

Guidelines designed to aid in the restoration of rare species have been previously proposed using two primary strategies to select individuals for augmentation and reintroduction: mixing progeny from different populations or separating individuals from different populations. Understanding the genetic structure and diversity of an endangered species can offer insights into conservation management strategies. We used random amplified polymorphic DNA markers to assess the genetic structure and diversity of Jacquemontia reclinata , a federally endangered species endemic to Southeastern Florida. We sampled 20 percent of total number of individuals from eight of the ten known wild populations. Across individuals high levels of polymorphic loci (94.7%) were found and larger populations had greater genetic diversity. Cluster and ordination analyses found that one population was genetically differentiated from all the others; this population grows in a unique habitat. Most genetic variation (77.5%) was found within populations, and genetic distances between populations were not explained by their geographic distances. We recommend the use of two management units in restoration programs for J. reclinata , one consisting of the genetically differentiated population and the second consisting of the other seven populations sampled.     

Use of Photo-Identification and Mark-Recapture Methodology to Assess Basking Shark (Cetorhinus maximus) Populations

Following centuries of exploitation, basking sharks (Cetorhinus maximus) are considered by IUCN as Endangered in the Northeast Atlantic, where they have now been substantially protected for over two decades. However, the present size of this population remains unknown. We investigated the use of photo-identification of individuals’ dorsal fins, combined with mark-recapture methodology, to investigate the size of populations of basking shark within the west coast of Scotland. From a total of 921 encounters photographed between 2004 and 2011, 710 sharks were found to be individually identifiable based on dorsal fin damage and natural features. Of these, only 41 individuals were re-sighted, most commonly both within days of, and close to the site of, the initial encounter. A smaller number were re-sighted after longer periods of up to two years. A comparison of the distinguishing features of individuals on first recording and subsequent re-sighting showed that in almost all cases these features remained little changed, suggesting the low re-sighting rate was not due to a loss of distinguishing features. Because of the low number of re-sighting we were not able to produce reliable estimates for the long-term regional population. However, for one 50 km diameter study area between the islands of Mull, Coll and Tiree, we were able to generate closed-population estimates for 6–9 day periods in 2010 of 985 (95% CI = 494–1683), and in 2011 of 201 (95% CI = 143–340). For the same 2011 period an open-population model generated a similar estimate of 213 (95% CI = 111–317). Otherwise the low rate and temporal patterning of re-sightings support the view that such local basking shark populations are temporary, dynamic groupings of individuals drawn from a much larger regional population than previously supposed. The study demonstrated the feasibility and limitations of photo-identification as a non-invasive technique for identifying individual basking sharks.