Parallel use of a shared genomic island of speciation in clinal and mosaic hybrid zones between cryptic seahorse lineages (original) (raw)
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2017
Diverging semi-isolated lineages either meet in narrow clinal hybrid zones, or have a mosaic distribution associated with environmental variation. Intrinsic reproductive isolation is often emphasized in the former and local adaptation in the latter, although both can contribute to isolation. Rarely these two patterns of spatial distribution are reported in the same study system. Here we report that the long-snouted seahorseHippocampus guttulatusis subdivided into discrete panmictic entities by both types of hybrid zones. Along the European Atlantic coasts, a northern and a southern lineage meet in the southwest of France where they coexist in sympatry with little hybridization. In the Mediterranean Sea, two lineages have a mosaic distribution, associated with lagoon-like and marine habitats. A fifth lineage was identified in the Black Sea. Genetic homogeneity over large spatial scales contrasts with isolation maintained in sympatry or close parapatry at a fine scale. A high variatio...
Biological Journal of the Linnean Society, 2020
The seahorse Hippocampus guttulatus reaches its highest abundance in confined environments, where it has unique biological and ecological traits that suggest significant genetic differentiation among populations. In the present study, we aimed to reveal the genetic structure of this species by analysing eight microsatellite loci and a mitochondrial DNA region (cytochrome b) of eight populations from the Central–Western Mediterranean Sea, including lagoon sites. Levels of genetic diversity, as measured by the total number of alleles, number of private alleles, allelic richness and heterozygosity, ranged from low to moderate. The overall value of inbreeding was high, indicating a deficiency in heterozygotes. The haplotype network had a star-like construction, with the most common haplotype present in all populations. Data from the two molecular markers congruently displayed a similar pattern and revealed low genetic differentiation, notwithstanding predictions based on species traits....
This first genetic study of Hippocampus hippocampus covers the species’ entire geographic range and employs two mtDNA markers (control region and cytochrome b) to establish patterns of population structuring. A total of 255 specimens from 21 locations were used to obtain 89 concatenated haplotypes. The common haplotype was present in all but one population, however, most haplotypes were unique. The haplotype network had a star-like construction, suggesting expansion from a bottleneck event. FST and AMOVA revealed population subdivision into three geographic regions (English Channel + Bay of Biscay, Mediterranean Sea + Atlantic Ocean Iberian coast + Macaronesian Islands, and West Africa) with barriers to gene flow indentified at Cape Finisterre and the Cape Verde frontal zone. Neutrality tests and nested clade analysis suggest a complex demographic history, with both historic events and contemporary processes shaping patterns of genetic differentiation. The genetic population subdivision detected in this study indicates that H. hippocampus should be managed as three separate units. This is especially pertinent as H. hippocampus populations within the West African region are the only ones known to be specifically targeted for exploitation.
Seahorses hold an iconic status and are popular exhibits in zoos and public aquaria, where they are often on display in multi-species systems. Two of the more popularly kept species are the lined seahorse, Hippocampus erectus, and the longsnout seahorse, H. reidi. These two species are from different evolutionary subclades, but can produce viable hybrid F1 offspring, therefore species segregation should be maintained for seahorse conservation breeding programs. Hybrid H. erectus ♂ × H. reidi ♀ F1 offspring exhibit higher median meristic counts for various traits, although large ranges in counts make it difficult to identify hybrids by meristics alone. A molecular protocol was developed to identify both the parent species, and the reciprocal hybrids using polymerase chain reaction restriction - fragment length polymorphism (PCR-RFLP). The PCR-RFLP protocol employed the use of the BsrBI and Ms1I restriction enzymes at the Tmo-4c4 and S7 loci, respectively. The developed protocol was e...
Marine dispersal and barriers drive Atlantic seahorse diversification
Aim- To investigate how marine barriers shaped the demographic history of Atlantic seahorses (Syngnathidae: Hippocampus). Location- Atlantic Ocean. Methods- Range-wide sampling (n = 390) at mitochondrial and up to five nuclear DNA loci was carried out across the Hippocampus erectus species complex (H. erectus from the Caribbean/North America, H. patagonicus from South America and H. hippocampus from Europe and West Africa). Multi-species coalescent and approximate Bayesian computation (ABC) frameworks were used to estimate support of competing biogeographical hypotheses and demographic parameters, including lineage divergence times, effective population sizes and magnitudes of population size change. Results- We identified four distinct lineages within the H. erectus complex. A posterior probability of 0.626 and corresponding Bayes factors ranging from 3.68 to 11.38 gave moderate to strong support for a basal divergence between South American populations of H. patagonicus and Caribbean/North American populations of H. erectus coincident with the inter-regional freshwater outflow of the Amazon River Barrier (ARB). Estimates of historical effective population sizes and divergence times indicate that European and West African populations of H. hippocampus expanded after colonization from a more demographically stable Caribbean/North American H. erectus. Main conclusions- Our findings of trans-Atlantic colonization followed by isolation across a deep oceanic divide, and isolation across a freshwater barrier, may demonstrate a contrast in marine divide permeability for this group of rafters. Demographic inference supports the establishment of an ancestral population of the H. erectus complex in the Americas, followed by the ARB splitting it into Caribbean/North and South American lineages at a time of increased sedimentation and outflow. Our estimates suggest that following this split, colonization occurred across the Atlantic via the Gulf Stream currents with subsequent trans-Atlantic isolation. These results illustrate that rafting can be a means of range expansion over large distances, but may be insufficient for sustaining genetic connectivity across major barriers, thereby resulting in lineage divergence.
Journal of Heredity, 2016
Isolated populations provide special opportunities to study local adaptation and incipient speciation. In some cases, however, morphological evolution can obscure the taxonomic status of recently founded populations. Here, we use molecular markers to show that an anchialinelake-restricted population of seahorses, originally identified as Hippocampus reidi, appears on the basis of DNA data to be Hippocampus erectus. We collected seahorses from Sweetings Pond, on Eleuthera Island, Bahamas, during the summer of 2014. We measured morphological traits and sequenced 2 genes, cytochrome b and ribosomal protein S7, from 19 seahorses in our sample. On the basis of morphology, Sweetings Pond seahorses could not be assigned definitively to either of the 2 species of seahorse, H. reidi and H. erectus, that occur in marine waters surrounding the Bahamas. However, our DNA-based phylogenetic analysis showed that the Sweetings Pond fish were firmly nested within the H. erectus clade with a Bayesian posterior probability greater than 0.99. Thus, Sweetings Pond seahorses most recently shared a common ancestor with H. erectus populations from the Western Atlantic. Interestingly, the seahorses from Sweetings Pond differ morphologically from other marine populations of H. erectus in having a more even torso to tail length ratio. The substantial habitat differences between Sweetings Pond and the surrounding coastal habitat make Sweetings Pond seahorses particularly interesting from the perspectives of conservation, local adaptation, and incipient speciation.
Conservation Genetics, 2007
The long-snouted seahorse Hippocampus guttulatus is one of the two European seahorse species. We describe the isolation of the first 12 microsatellite loci in this threatened species. These new markers were tested in non-invasive samples of 32 seahorses from NW Spain. The number of alleles ranged from 2 to 15 (mean: 6.3) and expected heterozygosity from 0.031 to 0.912 (mean: 0.500). All loci conformed to Hardy–Weinberg expectations and no genotypic disequilibrium was observed between any pair of loci. The theoretical exclusion probabilities for this set of loci, when no parental information exists or when one parent is known, were 0.973 and 0.998, respectively. This study indicates the usefulness of these novel loci for population analysis and kinship studies in Hippocampus guttulatus. Their potential application is extended to the other European seahorse species, since all loci were successfully cross-amplified in H. hippocampus.
Conservation Genetics, 2015
The effective design of species conservation and management programs is reliant on information such as extant geographic distribution, taxon-specific life-history characteristics, and the relative influence of historic processes and contemporary environmental parameters in shaping population genetic diversity. Seahorses are small coastal fish, weak swimmers as adults and with brooded young, limiting their dispersal potential. Seahorses live in sheltered locations, including estuaries which are physically isolated from each other. Therefore panmixia across their geographic range is unlikely. Hippocampus guttulatus, a seahorse inhabiting European waters, has a geographic range spanning a number of contemporary oceanographic features that are proposed barriers to gene flow. Thus this fish is well-placed to test the relative contributions of environment and life-history factors in shaping contemporary population structuring. This study found that mitochondrial DNA and nuclear DNA (microsatellite) genotype data are concordant in suggesting that, like many other small fishes in European waters, H. guttulatus extant populations expanded from at least one southern European refugial population. Subsequent population differentiation of four geographic lineages reflects contemporary oceanographic barriers to gene flow. Demographic analyses suggest a northward expansion from a southern refugium, and long-term isolation between Black Sea and Mediterranean Sea populations. Moreover H. guttulatus contemporary population distribution and population structure is predominately explained by historic and oceanographic influences, rather than life-history traits and associated habitat preference. These findings suggest that conservation of genetic diversity in H. guttulatus may be aided by a network of Marine Protected Areas (MPAs), implemented to conserve coastal species and habitats, but the species' unusual life history and gamete retaining behaviours should be considered as part of management decisions including MPA design and fisheries management plans.
Conservation Genetics, 2010
Understanding the population structure and evolutionary history of the eastern Pacific seahorse Hippocampus ingens is critical for the effective management of this threatened species. Life history characteristics of H. ingens (site fidelity and brooding of young) may limit gene flow and lead to population differentiation. A recent study analyzing conserved fragments of the mitochondrial cyt b and control region found no population structure. We reassess this conclusion with a phylogeographic analysis of relationships among 115 individuals of H. ingens over a broader geographic range (San Diego Bay in California, Gulf of California, Central America, Ecuador, and Peru) based on a more variable 428 base pair fragment of the control region. This expanded analysis affirms low overall nucleotide diversity relative to other seahorses (h p = 0.004), and shows evidence of a recent bottleneck and population expansion since the middle Pleistocene. AMOVA analysis shows moderate overall population structure (U ST = 0.10, P val = 0.00), and pairwise U ST estimates indicate structure between the Gulf of California and all Pacific coast localities. Knowledge of population structure in H. ingens may improve conservation efforts by identifying evolutionarily important management units, and could determine source regions in the continuing trade of seahorses for traditional Chinese medicine. The level of genetic divergence observed between the Gulf of California and all other localities sampled may distinguish the Gulf as a separate management unit. Additional phylogeographic research with more quickly evolving genetic markers and targeted sampling at the mouth of the Gulf of California is warranted to inform strategies for conservation of this threatened seahorse.