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Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era.

Gagnaire PA, Broquet T, Aurelle D, Viard F, Souissi A, Bonhomme F, Arnaud-Haond S, Bierne N - Evol Appl (2015)

Bottom Line: We highlight several issues that limit the effectiveness of methods based on neutral markers when there is virtually no genetic differentiation among samples.We argue that the increased ability to apply the concepts of cline analyses will improve dispersal inferences across physical and ecological barriers that reduce connectivity locally.We contend that one of the most promising applications of population genomics is the use of outlier loci to delineate relevant conservation units and related eco-geographic features across which connectivity can be measured.

View Article: PubMed Central - PubMed

Affiliation: Université de Montpellier Montpellier, France ; CNRS - Institut des Sciences de l'Evolution, UMR 5554 UM-CNRS-IRD-EPHE, Station Méditerranéenne de l'Environnement Littoral Sète, France.

ABSTRACT
Estimating the rate of exchange of individuals among populations is a central concern to evolutionary ecology and its applications to conservation and management. For instance, the efficiency of protected areas in sustaining locally endangered populations and ecosystems depends on reserve network connectivity. The population genetics theory offers a powerful framework for estimating dispersal distances and migration rates from molecular data. In the marine realm, however, decades of molecular studies have met limited success in inferring genetic connectivity, due to the frequent lack of spatial genetic structure in species exhibiting high fecundity and dispersal capabilities. This is especially true within biogeographic regions bounded by well-known hotspots of genetic differentiation. Here, we provide an overview of the current methods for estimating genetic connectivity using molecular markers and propose several directions for improving existing approaches using large population genomic datasets. We highlight several issues that limit the effectiveness of methods based on neutral markers when there is virtually no genetic differentiation among samples. We then focus on alternative methods based on markers influenced by selection. Although some of these methodologies are still underexplored, our aim was to stimulate new research to test how broadly they are applicable to nonmodel marine species. We argue that the increased ability to apply the concepts of cline analyses will improve dispersal inferences across physical and ecological barriers that reduce connectivity locally. We finally present how neutral markers hitchhiking with selected loci can also provide information about connectivity patterns within apparently well-mixed biogeographic regions. We contend that one of the most promising applications of population genomics is the use of outlier loci to delineate relevant conservation units and related eco-geographic features across which connectivity can be measured.

No MeSH data available.


Related in: MedlinePlus

Genomic islands of differentiation and the information therein. (A) A genomic island of differentiation between Atlantic and Mediterranean sea bass lineages (Dicentrarchus labrax) on chromosome 7 (RAD-sequencing data from Tine et al. 2014). (B) Geographic clines between two partially reproductively isolated species of sole, Solea senegalensis (Sp. 1, left side) and Solea aegyptiaca (Sp. 2, right side) assessed by RAD-Sequencing (A. Souissi, P.-A. Gagnaire, L. Bahri-Sfar, F. Bonhomme, unpublished). Red and orange clines correspond to expectations near reproductive isolation loci (i.e. at the center of a genomic island, where there is no introgression), for a diagnostic locus (red) and a locus only polymorphic in S. senegalensis (orange) due to incomplete lineage sorting. The green cline shows a gradient (or a tail) of introgression due to the inflow of S. aegyptiaca alleles in the S. senegalensis background. At this locus, the shared allele is a consequence of secondary introgression instead of incomplete lineage sorting. Such gradients of introgression are expected to be found at loci showing intermediate degrees of linkage with reproductive isolation loci (i.e. located in the periphery of a genomic island, where introgression is reduced but not zero). Introgression tails may be used to reveal cryptic genetic structure where freely recombining neutral loci remain uninformative (black dashed line), as it is the case in S. senegalensis.
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fig04: Genomic islands of differentiation and the information therein. (A) A genomic island of differentiation between Atlantic and Mediterranean sea bass lineages (Dicentrarchus labrax) on chromosome 7 (RAD-sequencing data from Tine et al. 2014). (B) Geographic clines between two partially reproductively isolated species of sole, Solea senegalensis (Sp. 1, left side) and Solea aegyptiaca (Sp. 2, right side) assessed by RAD-Sequencing (A. Souissi, P.-A. Gagnaire, L. Bahri-Sfar, F. Bonhomme, unpublished). Red and orange clines correspond to expectations near reproductive isolation loci (i.e. at the center of a genomic island, where there is no introgression), for a diagnostic locus (red) and a locus only polymorphic in S. senegalensis (orange) due to incomplete lineage sorting. The green cline shows a gradient (or a tail) of introgression due to the inflow of S. aegyptiaca alleles in the S. senegalensis background. At this locus, the shared allele is a consequence of secondary introgression instead of incomplete lineage sorting. Such gradients of introgression are expected to be found at loci showing intermediate degrees of linkage with reproductive isolation loci (i.e. located in the periphery of a genomic island, where introgression is reduced but not zero). Introgression tails may be used to reveal cryptic genetic structure where freely recombining neutral loci remain uninformative (black dashed line), as it is the case in S. senegalensis.

Mentions: These mechanisms show how much it is important to sample not only the whole distribution range of a species but also other divergent populations, or closely related species that live in parapatry or in sympatry before interpreting spatial genetic variation patterns (Gagnaire et al. 2011; Cullingham et al. 2013; Gosset and Bierne 2013). Now that NGS tools begin to reveal genomic islands of differentiation between cryptic species that were previously considered as populations of the same species (Hemmer-Hansen et al. 2013; Karlsen et al. 2013; Tine et al. 2014), polymorphisms located in the periphery of these islands may become a powerful new type of markers to infer connectivity within species, as illustrated in Fig. 4. Importantly, the spatial range of application of genomic-island associated loci could be large if markers are taken at various recombination distances from the central region of a genomic island of differentiation.


Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era.

Gagnaire PA, Broquet T, Aurelle D, Viard F, Souissi A, Bonhomme F, Arnaud-Haond S, Bierne N - Evol Appl (2015)

Genomic islands of differentiation and the information therein. (A) A genomic island of differentiation between Atlantic and Mediterranean sea bass lineages (Dicentrarchus labrax) on chromosome 7 (RAD-sequencing data from Tine et al. 2014). (B) Geographic clines between two partially reproductively isolated species of sole, Solea senegalensis (Sp. 1, left side) and Solea aegyptiaca (Sp. 2, right side) assessed by RAD-Sequencing (A. Souissi, P.-A. Gagnaire, L. Bahri-Sfar, F. Bonhomme, unpublished). Red and orange clines correspond to expectations near reproductive isolation loci (i.e. at the center of a genomic island, where there is no introgression), for a diagnostic locus (red) and a locus only polymorphic in S. senegalensis (orange) due to incomplete lineage sorting. The green cline shows a gradient (or a tail) of introgression due to the inflow of S. aegyptiaca alleles in the S. senegalensis background. At this locus, the shared allele is a consequence of secondary introgression instead of incomplete lineage sorting. Such gradients of introgression are expected to be found at loci showing intermediate degrees of linkage with reproductive isolation loci (i.e. located in the periphery of a genomic island, where introgression is reduced but not zero). Introgression tails may be used to reveal cryptic genetic structure where freely recombining neutral loci remain uninformative (black dashed line), as it is the case in S. senegalensis.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4561567&req=5

fig04: Genomic islands of differentiation and the information therein. (A) A genomic island of differentiation between Atlantic and Mediterranean sea bass lineages (Dicentrarchus labrax) on chromosome 7 (RAD-sequencing data from Tine et al. 2014). (B) Geographic clines between two partially reproductively isolated species of sole, Solea senegalensis (Sp. 1, left side) and Solea aegyptiaca (Sp. 2, right side) assessed by RAD-Sequencing (A. Souissi, P.-A. Gagnaire, L. Bahri-Sfar, F. Bonhomme, unpublished). Red and orange clines correspond to expectations near reproductive isolation loci (i.e. at the center of a genomic island, where there is no introgression), for a diagnostic locus (red) and a locus only polymorphic in S. senegalensis (orange) due to incomplete lineage sorting. The green cline shows a gradient (or a tail) of introgression due to the inflow of S. aegyptiaca alleles in the S. senegalensis background. At this locus, the shared allele is a consequence of secondary introgression instead of incomplete lineage sorting. Such gradients of introgression are expected to be found at loci showing intermediate degrees of linkage with reproductive isolation loci (i.e. located in the periphery of a genomic island, where introgression is reduced but not zero). Introgression tails may be used to reveal cryptic genetic structure where freely recombining neutral loci remain uninformative (black dashed line), as it is the case in S. senegalensis.
Mentions: These mechanisms show how much it is important to sample not only the whole distribution range of a species but also other divergent populations, or closely related species that live in parapatry or in sympatry before interpreting spatial genetic variation patterns (Gagnaire et al. 2011; Cullingham et al. 2013; Gosset and Bierne 2013). Now that NGS tools begin to reveal genomic islands of differentiation between cryptic species that were previously considered as populations of the same species (Hemmer-Hansen et al. 2013; Karlsen et al. 2013; Tine et al. 2014), polymorphisms located in the periphery of these islands may become a powerful new type of markers to infer connectivity within species, as illustrated in Fig. 4. Importantly, the spatial range of application of genomic-island associated loci could be large if markers are taken at various recombination distances from the central region of a genomic island of differentiation.

Bottom Line: We highlight several issues that limit the effectiveness of methods based on neutral markers when there is virtually no genetic differentiation among samples.We argue that the increased ability to apply the concepts of cline analyses will improve dispersal inferences across physical and ecological barriers that reduce connectivity locally.We contend that one of the most promising applications of population genomics is the use of outlier loci to delineate relevant conservation units and related eco-geographic features across which connectivity can be measured.

View Article: PubMed Central - PubMed

Affiliation: Université de Montpellier Montpellier, France ; CNRS - Institut des Sciences de l'Evolution, UMR 5554 UM-CNRS-IRD-EPHE, Station Méditerranéenne de l'Environnement Littoral Sète, France.

ABSTRACT
Estimating the rate of exchange of individuals among populations is a central concern to evolutionary ecology and its applications to conservation and management. For instance, the efficiency of protected areas in sustaining locally endangered populations and ecosystems depends on reserve network connectivity. The population genetics theory offers a powerful framework for estimating dispersal distances and migration rates from molecular data. In the marine realm, however, decades of molecular studies have met limited success in inferring genetic connectivity, due to the frequent lack of spatial genetic structure in species exhibiting high fecundity and dispersal capabilities. This is especially true within biogeographic regions bounded by well-known hotspots of genetic differentiation. Here, we provide an overview of the current methods for estimating genetic connectivity using molecular markers and propose several directions for improving existing approaches using large population genomic datasets. We highlight several issues that limit the effectiveness of methods based on neutral markers when there is virtually no genetic differentiation among samples. We then focus on alternative methods based on markers influenced by selection. Although some of these methodologies are still underexplored, our aim was to stimulate new research to test how broadly they are applicable to nonmodel marine species. We argue that the increased ability to apply the concepts of cline analyses will improve dispersal inferences across physical and ecological barriers that reduce connectivity locally. We finally present how neutral markers hitchhiking with selected loci can also provide information about connectivity patterns within apparently well-mixed biogeographic regions. We contend that one of the most promising applications of population genomics is the use of outlier loci to delineate relevant conservation units and related eco-geographic features across which connectivity can be measured.

No MeSH data available.


Related in: MedlinePlus