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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

Using the inflow of foreign alleles to reveal within-species connectivity patterns. At generation zero, two partially reproductively isolated species meet on a linear stepping-stone model between demes 10 and 11 and start to exchange genes. The auto-recruitment rate is 1 − m, and migration to adjacent demes is m/2 (with m = 0.5). A weak barrier to gene flow (m = 0.01) was set between demes 20 and 21, in the middle of the range of the species localized on the right side. Strong selection (s = 0.5) acts against heterozygote genotypes at a reproductive isolation locus, which is linked to neutral markers located at variable recombination distances (from closely linked to unlinked). A recombination rate of 1 cM per Mb was used to convert genetic into physical distances. (A) The step size, calculated as the difference in allele frequency between demes 20 and 21 (Δp), as a function of the number of generations postcontact. (B) Spatial allele frequency patterns after 10 000 generations of introgression showing the frequency step between demes 20 and 21. (C) The step size between demes 20 and 21 as a function of the physical distance to the reproductive isolation locus. (D) The step size between demes 20 and 21 as a function of the difference in allele frequency between species.
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fig03: Using the inflow of foreign alleles to reveal within-species connectivity patterns. At generation zero, two partially reproductively isolated species meet on a linear stepping-stone model between demes 10 and 11 and start to exchange genes. The auto-recruitment rate is 1 − m, and migration to adjacent demes is m/2 (with m = 0.5). A weak barrier to gene flow (m = 0.01) was set between demes 20 and 21, in the middle of the range of the species localized on the right side. Strong selection (s = 0.5) acts against heterozygote genotypes at a reproductive isolation locus, which is linked to neutral markers located at variable recombination distances (from closely linked to unlinked). A recombination rate of 1 cM per Mb was used to convert genetic into physical distances. (A) The step size, calculated as the difference in allele frequency between demes 20 and 21 (Δp), as a function of the number of generations postcontact. (B) Spatial allele frequency patterns after 10 000 generations of introgression showing the frequency step between demes 20 and 21. (C) The step size between demes 20 and 21 as a function of the physical distance to the reproductive isolation locus. (D) The step size between demes 20 and 21 as a function of the difference in allele frequency between species.

Mentions: Plots show the chromosomal and geographic signatures of selection under four different selective processes. Selected and neutral loci are colored in red and green, respectively. Genetic differentiation (FST) along the chromosome is measured between spatial coordinates −500 and 500. (A) A local adaptation cline lying at the frontier between two environments where selection acts in opposite directions (s = 0.1, σ = 30). The cline width parameter (w) is defined as the inverse of the maximum slope at the cline center, and k is a coefficient that depends on the selection regime (Slatkin 1973; Nagylaki 1975; Endler 1977; Barton and Gale 1993; Kruuk et al. 1999). A neutral hitchhiker locus with a recombination rate r with the selected locus makes a shift (Δp) in the central region of the cline, and an external gradient of allele frequency (∂p/∂x) directly outside the cline (Barton 1979b). (B) Hybrid zone cline between two partially reproductively isolated populations with selection acting against hybrid genotypes (s = 0.5). The amount of linkage disequilibrium (D) between selected loci is measured after dispersal at the center of the overlapping clines. (C) A tail of introgression produced by the inflow of foreign alleles entering a subdivided population (see Fig 3 for details). (D) Local connectivity patterns revealed by a global sweep. An unconditionally favorable mutation (s = 0.05) appears on the left side of a chain of demes (at an initial frequency of 1/2Ne) and then propagates to the right side from deme to deme (m = 0.01), leaving behind a complex allele frequency pattern at a neutral hitchhiking locus (r = 0.001). Local connectivity between adjacent demes is transiently revealed by the structure of the neutral hitchhiking locus, as long as gene flow re-homogenizes allele frequencies. The chromosomal signatures of selection can take the form of narrow regions of differentiation (A), large genomic islands (B), or shoulders of differentiation (C and D) centered on the selected loci.


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)

Using the inflow of foreign alleles to reveal within-species connectivity patterns. At generation zero, two partially reproductively isolated species meet on a linear stepping-stone model between demes 10 and 11 and start to exchange genes. The auto-recruitment rate is 1 − m, and migration to adjacent demes is m/2 (with m = 0.5). A weak barrier to gene flow (m = 0.01) was set between demes 20 and 21, in the middle of the range of the species localized on the right side. Strong selection (s = 0.5) acts against heterozygote genotypes at a reproductive isolation locus, which is linked to neutral markers located at variable recombination distances (from closely linked to unlinked). A recombination rate of 1 cM per Mb was used to convert genetic into physical distances. (A) The step size, calculated as the difference in allele frequency between demes 20 and 21 (Δp), as a function of the number of generations postcontact. (B) Spatial allele frequency patterns after 10 000 generations of introgression showing the frequency step between demes 20 and 21. (C) The step size between demes 20 and 21 as a function of the physical distance to the reproductive isolation locus. (D) The step size between demes 20 and 21 as a function of the difference in allele frequency between species.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig03: Using the inflow of foreign alleles to reveal within-species connectivity patterns. At generation zero, two partially reproductively isolated species meet on a linear stepping-stone model between demes 10 and 11 and start to exchange genes. The auto-recruitment rate is 1 − m, and migration to adjacent demes is m/2 (with m = 0.5). A weak barrier to gene flow (m = 0.01) was set between demes 20 and 21, in the middle of the range of the species localized on the right side. Strong selection (s = 0.5) acts against heterozygote genotypes at a reproductive isolation locus, which is linked to neutral markers located at variable recombination distances (from closely linked to unlinked). A recombination rate of 1 cM per Mb was used to convert genetic into physical distances. (A) The step size, calculated as the difference in allele frequency between demes 20 and 21 (Δp), as a function of the number of generations postcontact. (B) Spatial allele frequency patterns after 10 000 generations of introgression showing the frequency step between demes 20 and 21. (C) The step size between demes 20 and 21 as a function of the physical distance to the reproductive isolation locus. (D) The step size between demes 20 and 21 as a function of the difference in allele frequency between species.
Mentions: Plots show the chromosomal and geographic signatures of selection under four different selective processes. Selected and neutral loci are colored in red and green, respectively. Genetic differentiation (FST) along the chromosome is measured between spatial coordinates −500 and 500. (A) A local adaptation cline lying at the frontier between two environments where selection acts in opposite directions (s = 0.1, σ = 30). The cline width parameter (w) is defined as the inverse of the maximum slope at the cline center, and k is a coefficient that depends on the selection regime (Slatkin 1973; Nagylaki 1975; Endler 1977; Barton and Gale 1993; Kruuk et al. 1999). A neutral hitchhiker locus with a recombination rate r with the selected locus makes a shift (Δp) in the central region of the cline, and an external gradient of allele frequency (∂p/∂x) directly outside the cline (Barton 1979b). (B) Hybrid zone cline between two partially reproductively isolated populations with selection acting against hybrid genotypes (s = 0.5). The amount of linkage disequilibrium (D) between selected loci is measured after dispersal at the center of the overlapping clines. (C) A tail of introgression produced by the inflow of foreign alleles entering a subdivided population (see Fig 3 for details). (D) Local connectivity patterns revealed by a global sweep. An unconditionally favorable mutation (s = 0.05) appears on the left side of a chain of demes (at an initial frequency of 1/2Ne) and then propagates to the right side from deme to deme (m = 0.01), leaving behind a complex allele frequency pattern at a neutral hitchhiking locus (r = 0.001). Local connectivity between adjacent demes is transiently revealed by the structure of the neutral hitchhiking locus, as long as gene flow re-homogenizes allele frequencies. The chromosomal signatures of selection can take the form of narrow regions of differentiation (A), large genomic islands (B), or shoulders of differentiation (C and D) centered on the selected loci.

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