Dataset Information

Divergent Allometric Trajectories in Gene Expression and Coexpression Produce Species Differences in Sympatrically Speciating Midas Cichlid Fish.

ABSTRACT: The mechanisms of speciation without geographic isolation (i.e., sympatric speciation) remain debated. This is due in part to the fact that the genomic landscape that could promote or hinder species divergence in the presence of gene flow is still largely unknown. However, intensive research is now centered on understanding the genetic architecture of adaptive traits associated with this process as well as how gene expression might affect these traits. Here, using RNA-Seq data, we investigated gene expression of sympatrically speciating benthic and limnetic Neotropical cichlid fishes at two developmental stages. First, we identified groups of coexpressed genes (modules) at each stage. Although there are a few large and well-preserved modules, most of the other modules are not preserved across life stages. Second, we show that later in development more and larger coexpression modules are associated with divergence between benthic and limnetic fish compared with the earlier life stage. This divergence between benthic and limnetic fish in coexpression mirrors divergence in overall expression between benthic and limnetic fish, which is more pronounced later in life. Our results reveal that already at 1-day posthatch benthic and limnetic fish diverge in (co)expression, and that this divergence becomes more substantial when fish are free-swimming but still unlikely to have divergent swimming and feeding habits. More importantly, our study describes how the coexpression of several genes through development, as opposed to individual genes, is associated with benthic-limnetic species differences, and how two morphogenetic trajectories diverge as fish grow older.

SUBMITTER: Fruciano C

PROVIDER: S-EPMC6563553 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Divergent Allometric Trajectories in Gene Expression and Coexpression Produce Species Differences in Sympatrically Speciating Midas Cichlid Fish.

Fruciano Carmelo C Meyer Axel A Franchini Paolo P

Genome biology and evolution 20190601 6

The mechanisms of speciation without geographic isolation (i.e., sympatric speciation) remain debated. This is due in part to the fact that the genomic landscape that could promote or hinder species divergence in the presence of gene flow is still largely unknown. However, intensive research is now centered on understanding the genetic architecture of adaptive traits associated with this process as well as how gene expression might affect these traits. Here, using RNA-Seq data, we investigated g ...[more]

PMID: 31124568

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Project description:Established empirical cases of sympatric speciation are scarce, although there is an increasing consensus that sympatric speciation might be more common than previously thought. Midas cichlid fish are one of the few substantiated cases of sympatric speciation, and they formed repeated radiations in crater lakes. In contrast, in the same environment, such radiation patterns have not been observed in other species of cichlids and other families of fish. We analyze morphological and genetic variation in a cichlid species (Archocentrus centrarchus) that co-inhabits several crater lakes with the Midas species complex. In particular, we analyze variation in body and pharyngeal jaw shape (two ecologically important traits in sympatrically divergent Midas cichlids) and relate that to genetic variation in mitochondrial control region and microsatellites. Using these four datasets, we analyze variation between and within two Nicaraguan lakes: a crater lake where multiple Midas cichlids have been described and a lake where the source population lives. We do not observe any within-lake clustering consistent across morphological traits and genetic markers, suggesting the absence of sympatric divergence in A. centrarchus. Genetic differentiation between lakes was low and morphological divergence absent. Such morphological similarity between lakes is found not only in average morphology, but also when analyzing covariation between traits and degree of morphospace occupation. A combined analysis of the mitochondrial control region in A. centrarchus and Midas cichlids suggests that a difference between lineages in the timing of crater lake colonization cannot be invoked as an explanation for the difference in their levels of diversification. In light of our results, A. centrarchus represents the ideal candidate to study the genomic differences between these two lineages that might explain why some lineages are more likely to speciate and diverge in sympatry than others.

Project description:BackgroundSpeciation often occurs in complex or uncertain temporal and spatial contexts. Processes such as reinforcement, allopatric divergence, and assortative mating can proceed at different rates and with different strengths as populations diverge. The Central American Midas cichlid fish species complex is an important case study for understanding the processes of speciation. Previous analyses have demonstrated that allopatric processes led to species formation among the lakes of Nicaragua as well as sympatric speciation that is occurring within at least one crater lake. However, since speciation is an ongoing process and sampling genetic diversity of such lineages can be biased by collection scheme or random factors, it is important to evaluate the robustness of conclusions drawn on individual time samples.ResultsIn order to assess the validity and reliability of inferences based on different genetic samples, we have analyzed fish from several lakes in Nicaragua sampled at three different times over 16 years. In addition, this time series allows us to analyze the population genetic changes that have occurred between lakes, where allopatric speciation has operated, as well as between different species within lakes, some of which have originated by sympatric speciation. Focusing on commonly used genetic markers, we have analyzed both DNA sequences from the complete mitochondrial control region as well as nuclear DNA variation at ten microsatellite loci from these populations, sampled thrice in a 16 year time period, to develop a robust estimate of the population genetic history of these diversifying lineages.ConclusionThe conclusions from previous work are well supported by our comprehensive analysis. In particular, we find that the genetic diversity of derived crater lake populations is lower than that of the source population regardless of when and how each population was sampled. Furthermore, changes in various estimates of genetic diversity within lakes are minimal and provide no evidence for drastic changes during the last 20 years, supporting the hypothesis that the processes which have resulted in rapid speciation are primarily historical. In contrast, there is some evidence for ongoing evolution, particularly selection, in all lakes except crater Lake Masaya, perhaps reflecting the persistence of speciational processes. Importantly, we find that the crater Lake Apoyo population, for which strong evidence of sympatric speciation has been demonstrated, has lower genetic diversity than other crater lakes and the strongest evidence for ongoing selection.

Dataset Information

Divergent Allometric Trajectories in Gene Expression and Coexpression Produce Species Differences in Sympatrically Speciating Midas Cichlid Fish.

Publications

Divergent Allometric Trajectories in Gene Expression and Coexpression Produce Species Differences in Sympatrically Speciating Midas Cichlid Fish.

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