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Speciation-by-depth on coral reefs: Sympatric divergence with gene flow or cryptic transient isolation?

ABSTRACT: The distributions of many sister species in the sea overlap geographically but are partitioned along depth gradients. The genetic changes leading to depth segregation may evolve in geographic isolation as a prerequisite to coexistence or may emerge during primary divergence leading to new species. These alternatives can now be distinguished via the power endowed by the thousands of scorable loci provided by second-generation sequence data. Here, we revisit the case of two depth-segregated, genetically isolated ecotypes of the nominal Caribbean candelabrum coral Eunicea flexuosa. Previous analyses based on a handful of markers could not distinguish between models of genetic exchange after a period of isolation (consistent with secondary contact) and divergence with gene flow (consistent with primary divergence). Analyses of the history of isolation, genetic exchange and population size based on 15,640 new SNP markers derived from RNAseq data best support models where divergence began 800K BP and include epochs of divergence with gene flow, but with an intermediate period of transient isolation. Results also supported the previous conclusion that recent exchange between the ecotypes occurs asymmetrically from the Shallow lineage to the Deep. Parallel analyses of data from two other corals with depth-segregated populations (Agaricia fragilis and Pocillopora damicornis) suggest divergence leading to depth-segregated populations may begin with a period of symmetric exchange, but that an epoch of population isolation precedes more complete isolation marked by asymmetric introgression. Thus, while divergence-with-gene flow may account for much of the differentiation that separates closely related, depth-segregated species, it remains to be seen whether any critical steps in the speciation process only occur when populations are isolated.

SUBMITTER: Prada C

PROVIDER: S-EPMC7894305 | biostudies-literature | 2021 Jan

REPOSITORIES: biostudies-literature

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Speciation-by-depth on coral reefs: Sympatric divergence with gene flow or cryptic transient isolation?

Prada Carlos C Hellberg Michael E ME

Journal of evolutionary biology 20201120 1

The distributions of many sister species in the sea overlap geographically but are partitioned along depth gradients. The genetic changes leading to depth segregation may evolve in geographic isolation as a prerequisite to coexistence or may emerge during primary divergence leading to new species. These alternatives can now be distinguished via the power endowed by the thousands of scorable loci provided by second-generation sequence data. Here, we revisit the case of two depth-segregated, genet ...[more]

PMID: 33140895

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Project description:Niche partitioning and sequence evolution drive genomic and phenotypic divergence, which ultimately leads to bacterial diversification. This study investigated the genomic composition of two Shewanella baltica clades previously identified through multilocus sequencing typing and recovered from the redox transition zone in the central Baltic Sea. Comparative genomic analysis revealed significantly higher interclade than intraclade genomic dissimilarity and that a subset of genes present in clade A were associated with potential adaptation to respiration of sulfur compounds present in the redox transition zone. The transcriptomic divergence between two representative strains of clades A and D, OS185 and OS195, was also characterized and revealed marked regulatory differences. We found that both the transcriptional divergence of shared genes and expression of strain-specific genes led to differences in regulatory patterns between strains that correlate with environmental redox niches. For instance, under anoxic conditions of respiratory nitrate ammonification, OS185-the strain isolated from a nitrate-rich environment-upregulated nearly twice the number of shared genes upregulated by OS195-the strain isolated from an H2S-containing anoxic environment. Conversely, OS195 showed stronger induction of strain-specific genes, especially those associated with sulfur compound respiration, under thiosulfate-reducing conditions. A positive association between the level of transcriptional divergence and the level of sequence divergence for shared genes was also noted. Our results provide further support for the hypothesis that genomic changes impacting transcriptional regulation play an important role in the diversification of ecologically distinct populations.IMPORTANCE This study examined potential mechanisms through which co-occurring Shewanella baltica strains diversified to form ecologically distinct populations. At the time of isolation, the strains studied composed the major fraction of culturable nitrate-reducing communities in the Baltica Sea. Analysis of genomic content of 13 S. baltica strains from two clades representing different ecotypes demonstrated that one clade specifically possesses a number of genes that could favor successful adaptation to respire sulfur compounds in the portion of the water column from which these strains were isolated. In addition, transcriptional profiling of fully sequenced strains representative of these two clades, OS185 and OS195, under oxygen-, nitrate-, and thiosulfate-respiring conditions demonstrated that the strains exhibit relatively similar transcriptional responses during aerobic growth but more-distinct transcriptional responses under nitrate- and thiosulfate-respiring conditions. Results from this study provide insights into how genomic and gene regulatory diversification together impacted the redox specialization of the S. baltica strains.

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Speciation-by-depth on coral reefs: Sympatric divergence with gene flow or cryptic transient isolation?

Publications

Speciation-by-depth on coral reefs: Sympatric divergence with gene flow or cryptic transient isolation?

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