Past volcanic activity predisposes an endemic threatened seabird to negative anthropogenic impacts.

Humans are regularly cited as the main driver of current biodiversity extinction, but the impact of historic volcanic activity is often overlooked. Pre-human evidence of wildlife abundance and diversity are essential for disentangling anthropogenic impacts from natural events. Réunion Island, with its intense and well-documented volcanic activity, endemic biodiversity, long history of isolation and recent human colonization, provides an opportunity to disentangle these processes. We track past demographic changes of a critically endangered seabird, the Mascarene petrel Pseudobulweria aterrima, using genome-wide SNPs. Coalescent modeling suggested that a large ancestral population underwent a substantial population decline in two distinct phases, ca. 125,000 and 37,000 years ago, coinciding with periods of major eruptions of Piton des Neiges. Subsequently, the ancestral population was fragmented into the two known colonies, ca. 1500 years ago, following eruptions of Piton de la Fournaise. In the last century, both colonies declined significantly due to anthropogenic activities, and although the species was initially considered extinct, it was rediscovered in the 1970s. Our findings suggest that the current conservation status of wildlife on volcanic islands should be firstly assessed as a legacy of historic volcanic activity, and thereafter by the increasing anthropogenic impacts, which may ultimately drive species towards extinction.

Stepping up to genome scan allows stock differentiation in the worldwide distributed blue shark Prionace glauca.

The blue shark Prionace glauca is a top predator with one of the widest geographical distributions of any shark species. It is classified as Critically Endangered in the Mediterranean Sea, and Near Threatened globally. Previous genetic studies did not reject the null hypothesis of a single global population. The blue shark was proposed as a possible archetype of the "grey zone of population differentiation," coined to designate cases where population structure may be too recent or too faint to be detected using a limited set of markers. Here, blue shark samples collected throughout its global range were sequenced using a specific RAD method (DArTseq), which recovered 37,655 genome-wide single nucleotide polymorphisms (SNPs). Two main groups emerged, with Mediterranean Sea and northern Atlantic samples (Northern population) differentiated significantly from the Indo-west Pacific samples (Southern population). Significant pairwise FST values indicated further genetic differentiation within the Atlantic Ocean, and between the Atlantic Ocean and the Mediterranean Sea. Reconstruction of recent demographic history suggested divergence between Northern and Southern populations occurred about 500 generations ago and revealed a drastic reduction in effective population size from a large ancestral population. Our results illustrate the power of genome scans to detect population structure and reconstruct demographic history in highly migratory marine species. Given that the management plans of the blue shark (targeted or bycatch) fisheries currently assume panmictic regional stocks, we strongly recommend that the results presented here be considered in future stock assessments and conservation strategies.

Connectivity and population structure of albacore tuna across southeast Atlantic and southwest Indian Oceans inferred from multidisciplinary methodology.

Albacore tuna (Thunnus alalunga) is an important target of tuna fisheries in the Atlantic and Indian Oceans. The commercial catch of albacore is the highest globally among all temperate tuna species, contributing around 6% in weight to global tuna catches over the last decade. The accurate assessment and management of this heavily exploited resource requires a robust understanding of the species' biology and of the pattern of connectivity among oceanic regions, yet Indian Ocean albacore population dynamics remain poorly understood and its level of connectivity with the Atlantic Ocean population is uncertain. We analysed morphometrics and genetics of albacore (n = 1,874) in the southwest Indian (SWIO) and southeast Atlantic (SEAO) Oceans to investigate the connectivity and population structure. Furthermore, we examined the species' dispersal potential by modelling particle drift through major oceanographic features. Males appear larger than females, except in South African waters, yet the length-weight relationship only showed significant male-female difference in one region (east of Madagascar and Reunion waters). The present study produced a genetic differentiation between the southeast Atlantic and southwest Indian Oceans, supporting their demographic independence. The particle drift models suggested dispersal potential of early life stages from SWIO to SEAO and adult or sub-adult migration from SEAO to SWIO.

Evolutionary history of a Scottish harbour seal population.

Efforts to conserve marine mammals are often constrained by uncertainty over their population history. Here, we examine the evolutionary history of a harbour seal (Phoca vitulina) population in the Moray Firth, northeast Scotland using genetic tools and microsatellite markers to explore population change. Previous fine-scale analysis of UK harbour seal populations revealed three clusters in the UK, with a northeastern cluster that included our Moray Firth study population. Our analysis revealed that the Moray Firth cluster is an independent genetic group, with similar levels of genetic diversity across each of the localities sampled. These samples were used to assess historic abundance and demographic events in the Moray Firth population. Estimates of current genetic diversity and effective population size were low, but the results indicated that this population has remained at broadly similar levels following the population bottleneck that occurred after post-glacial recolonization of the area.

Speciation history of European (Anguilla anguilla) and American eel (A. rostrata), analysed using genomic data.

Speciation in the ocean could differ from terrestrial environments due to fewer barriers to gene flow. Hence, sympatric speciation might be common, with American and European eel being candidates for exemplifying this. They show disjunct continental distributions on both sides of the Atlantic, but spawn in overlapping regions of the Sargasso Sea from where juveniles are advected to North American, European and North African coasts. Hybridization and introgression are known to occur, with hybrids almost exclusively observed in Iceland. Different speciation scenarios have been suggested, involving either vicariance or sympatric ecological speciation. Using RAD sequencing and whole-genome sequencing data from parental species and F1 hybrids, we analysed speciation history based on the joint allele frequency spectrum (JAFS) and pairwise sequentially Markovian coalescent (PSMC) plots. JAFS supported a model involving a split without gene flow 150,000-160,000 generations ago, followed by secondary contact 87,000-92,000 generations ago, with 64% of the genome experiencing restricted gene flow. This supports vicariance rather than sympatric speciation, likely associated with Pleistocene glaciation cycles and ocean current changes. Whole-genome PSMC analysis of F1 hybrids from Iceland suggested divergence 200,000 generations ago and indicated subsequent gene flow rather than strict isolation. Finally, simulations showed that results from both approaches (JAFS and PSMC) were congruent. Hence, there is strong evidence against sympatric speciation in North Atlantic eels. These results reiterate the need for careful consideration of cases of possible sympatric speciation, as even in seemingly barrier-free oceanic environments palaeoceanographic factors may have promoted vicariance and allopatric speciation.

Chemical contaminants (trace metals, persistent organic pollutants) in albacore tuna from western Indian and south-eastern Atlantic Oceans: Trophic influence and potential as tracers of populations.

Albacore tuna (Thunnus alalunga) is a highly commercial fish species harvested in the world's Oceans. Identifying the potential links between populations is one of the key tools that can improve the current management across fisheries areas. In addition to characterising populations' contamination state, chemical compounds can help refine foraging areas, individual flows and populations' structure, especially when combined with other intrinsic biogeochemical (trophic) markers such as carbon and nitrogen stable isotopes. This study investigated the bioaccumulation of seven selected trace metals - chromium, nickel, copper (Cu), zinc (Zn), cadmium (Cd), mercury (Hg) and lead - in the muscle of 443 albacore tunas, collected over two seasons and/or years in the western Indian Ocean (WIO: Reunion Island and Seychelles) and in the south-eastern Atlantic Ocean (SEAO: South Africa). The main factor that explained metal concentration variability was the geographic origin of fish, rather than the size and the sex of individuals, or the season/year of sampling. The elements Cu, Zn, Cd and Hg indicated a segregation of the geographic groups most clearly. For similar sized-individuals, tunas from SEAO had significantly higher concentrations in Cu, Zn and Cd, but lower Hg concentrations than those from WIO. Information inferred from the analysis of trophic markers (δ13C, δ15N) and selected persistent organic pollutants, as well as information on stomach contents, corroborated the geographical differences obtained by trace metals. It also highlighted the influence of trophic ecology on metal bioaccumulation. Finally, this study evidenced the potential of metals and chemical contaminants in general as tracers, by segregating groups of individuals using different food webs or habitats, to better understand spatial connectivity at the population scale. Limited flows of individuals between the SEAO and the WIO are suggested. Albacore as predatory fish also provided some information on environmental and food web chemical contamination in the different study areas.

Reproductive Biology of Albacore Tuna (Thunnus alalunga) in the Western Indian Ocean.

The reproductive biology of albacore tuna, Thunnus alalunga, in the western Indian Ocean was examined through analysis of the sex ratio, spawning season, length-at-maturity (L50), spawning frequency and fecundity. From 2013 to 2015, a total of 923 female and 867 male albacore were sampled. A bias in sex ratio was found in favor of females with fork length (LF) < 100 cm. Using histological analyses and gonadosomatic index, spawning was found to occur between 10°S and 30°S, mainly to the east of Madagascar from October to January. Large females contributed more to reproduction through their longer spawning period compared to small individuals. The L50 (mean ± standard error) of female albacore was estimated at 85.3 ± 0.7 cm LF. Albacore spawn on average every 2.2 days within the spawning region and spawning months, from November to January. Batch fecundity ranged between 0.26 and 2.09 million oocytes and the relative batch fecundity (mean ± standard deviation) was estimated at 53.4 ± 23.2 oocytes g-1 of somatic-gutted weight. The study provides new information on the reproductive development and classification of albacore in the western Indian Ocean. The reproductive parameters will reduce uncertainty in current stock assessment models which will eventually assist the fishery to be sustainable for future generations.

Discovery of Genome-Wide Microsatellite Markers in Scombridae: A Pilot Study on Albacore Tuna.

Recent developments in sequencing technologies and bioinformatics analysis provide a greater amount of DNA sequencing reads at a low cost. Microsatellites are the markers of choice for a variety of population genetic studies, and high quality markers can be discovered in non-model organisms, such as tuna, with these recent developments. Here, we use a high-throughput method to isolate microsatellite markers in albacore tuna, Thunnus alalunga, based on coupling multiplex enrichment and next-generation sequencing on 454 GS-FLX Titanium pyrosequencing. The crucial minimum number of polymorphic markers to infer evolutionary and ecological processes for this species has been described for the first time. We provide 1670 microsatellite design primer pairs, and technical and molecular genetics selection resulting in 43 polymorphic microsatellite markers. On this panel, we characterized 34 random and selectively neutral markers («neutral¼) and 9 «non-neutral¼ markers. The variability of «neutral¼ markers was screened with 136 individuals of albacore tuna from southwest Indian Ocean (42), northwest Indian Ocean (31), South Africa (31), and southeast Atlantic Ocean (32). Power analysis demonstrated that the panel of genetic markers can be applied in diversity and population genetics studies. Global genetic diversity for albacore was high with a mean number of alleles at 16.94; observed heterozygosity 66% and expected heterozygosity 77%. The number of individuals was insufficient to provide accurate results on differentiation. Of the 9 «non-neutral¼ markers, 3 were linked to a sequence of known function. The one is located to a sequence having an immunity function (ThuAla-Tcell-01) and the other to a sequence having energy allocation function (ThuAla-Hki-01). These two markers were genotyped on the 136 individuals and presented different diversity levels. ThuAla-Tcell-01 has a high number of alleles (20), heterozygosity (87-90%), and assignment index. ThuAla-Hki-01 has a lower number of alleles (9), low heterozygosity (24-27%), low assignment index and significant inbreeding. Finally, the 34 «neutral¼ and 3 «non-neutral¼ microsatellites markers were tested on four economically important Scombridae species-Thunnus albacares, Thunnus thynnus, Thunnus obesus, and Acanthocybium solandri.

Detecting past changes of effective population size.

Understanding and predicting population abundance is a major challenge confronting scientists. Several genetic models have been developed using microsatellite markers to estimate the present and ancestral effective population sizes. However, to get an overview on the evolution of population requires that past fluctuation of population size be traceable. To address the question, we developed a new model estimating the past changes of effective population size from microsatellite by resolving coalescence theory and using approximate likelihoods in a Monte Carlo Markov Chain approach. The efficiency of the model and its sensitivity to gene flow and to assumptions on the mutational process were checked using simulated data and analysis. The model was found especially useful to provide evidence of transient changes of population size in the past. The times at which some past demographic events cannot be detected because they are too ancient and the risk that gene flow may suggest the false detection of a bottleneck are discussed considering the distribution of coalescence times. The method was applied on real data sets from several Atlantic salmon populations. The method called VarEff (Variation of Effective size) was implemented in the R package VarEff and is made available at https://qgsp.jouy.inra.fr and at http://cran.r-project.org/web/packages/VarEff.

Changes in the genetic structure of Atlantic salmon populations over four decades reveal substantial impacts of stocking and potential resiliency.

While the stocking of captive-bred fish has been occurring for decades and has had substantial immediate genetic and evolutionary impacts on wild populations, its long-term consequences have only been weakly investigated. Here, we conducted a spatiotemporal analysis of 1428 Atlantic salmon sampled from 1965 to 2006 in 25 populations throughout France to investigate the influence of stocking on the neutral genetic structure in wild Atlantic salmon (Salmo salar) populations. On the basis of the analysis of 11 microsatellite loci, we found that the overall genetic structure among populations dramatically decreased over the period studied. Admixture rates among populations were highly variable, ranging from a nearly undetectable contribution from donor stocks to total replacement of the native gene pool, suggesting extremely variable impacts of stocking. Depending on population, admixture rates either increased, remained stable, or decreased in samples collected between 1998 and 2006 compared to samples from 1965 to 1987, suggesting either rising, long-lasting or short-term impacts of stocking. We discuss the potential mechanisms contributing to this variability, including the reduced fitness of stocked fish and persistence of wild locally adapted individuals.

The distribution of coalescence times and distances between microsatellite alleles with changing effective population size.

We investigate the effects of past changes of the effective population size on the present allelic diversity at a microsatellite marker locus. We first derive the analytical expression of the generating function of the joint probabilities of the time to the Most Recent Common Ancestor for a pair of alleles and of their distance (the difference in allele size). We give analytical solutions in the case of constant population size and the geometrical mutation model. Otherwise, numerical inversion allows the distributions to be calculated in general cases. The effects of population expansion or decrease and the possibility to detect an ancient bottleneck are discussed. The method is extended to samples of three and four alleles, which allows investigating the covariance structure of the frequencies f(k) of pairs of alleles with a size difference of k motifs, and suggesting some approaches to the estimation of past demography.

What do artificial neural networks tell us about the genetic structure of populations? The example of European pig populations.

General and genetic statistical methods are commonly used to deal with microsatellite data (highly variable neutral genetic markers). In this paper, the self-organizing map (SOM) that belongs to the unsupervised artificial neural networks (ANNs) was applied to analyse the structure of 58 European and two Chinese pig populations (Sus scrofa) including commercial lines, local breeds and cosmopolitan breeds. Results were compared with other unsupervised classification or ordination methods such as factorial correspondence analysis, hierarchical clustering from an allele sharing distance and the Bayesian genetic model and with principal components analysis and neighbour joining from allelic frequencies and genetic distances between populations. Like other methods, SOMs were able to classify individuals according to their breed origin and to visualize similarities between breeds. They provided additional information on the within- and between-population diversity, allowed differences between similar populations to be highlighted and helped differentiate different groups of populations.

An examination of genetic diversity and effective population size in Atlantic salmon populations.

Effective population size (Ne) is an important parameter in the conservation of genetic diversity. Comparative studies of empirical data that gauge the relative accuracy of Ne methods are limited, and a better understanding of the limitations and potential of Ne estimators is needed. This paper investigates genetic diversity and Ne in four populations of wild anadromous Atlantic salmon (Salmo salar L.) in Europe, from the Rivers Oir and Scorff (France) and Spey and Shin (Scotland). We aimed to understand present diversity and historical processes influencing current population structure. Our results showed high genetic diversity for all populations studied, despite their wide range of current effective sizes. To improve understanding of high genetic diversity observed in the populations with low effective size, we developed a model predicting present diversity as a function of past demographic history. This suggested that high genetic diversity could be explained by a bottleneck occurring within recent centuries rather than by gene flow. Previous studies have demonstrated the efficiency of coalescence models to estimate Ne. Using nine subsets from 37 microsatellite DNA markers from the four salmon populations, we compared three coalescence estimators based on single and dual samples. Comparing Ne estimates confirmed the efficiency of increasing the number and variability of microsatellite markers. This efficiency was more accentuated for the smaller populations. Analysis with low numbers of neutral markers revealed uneven distributions of allelic frequencies and overestimated short-term Ne. In addition, we found evidence of artificial stock enhancement using native and non-native origin. We propose estimates of Ne for the four populations, and their applications for salmon conservation and management are discussed.