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Ecological selection as the cause and sexual differentiation as the consequence of species divergence?

ABSTRACT: Key conceptual issues about speciation go unanswered without consideration of non-mutually exclusive factors. With tests based on speciation theory, we exploit the island distribution and habitat differences exhibited by the Caribbean cricket Amphiacusta sanctaecrucis, and with an analysis of divergent ecological selection, sexually selected differentiation and geographical isolation, address how these different factors interact. After testing for divergent selection by comparing neutral genetic and morphological divergence in one ecological (mandible shape) and one sexual (male genitalia shape) trait, we examine whether ecological or sexual selection is the primary mechanism driving population divergence. We find that all three factors--isolation, ecological and sexual selection--contribute to divergence, and that their interaction determines the stage of completeness achieved during the speciation process, as measured by patterns of genetic differentiation. Moreover, despite the striking diversity in genitalic shapes across the genus Amphiacusta, which suggests that sexual selection drives speciation, the significant differences in genitalia shape between forest habitats revealed here implies that ecological divergence may be the primary axis of divergence. Our work highlights critical unstudied aspects in speciation-differentiating the cause from the consequence of divergence-and suggests avenues for further disentangling the roles of natural and sexual selection in driving divergence in Amphiacusta.

SUBMITTER: Oneal E

PROVIDER: S-EPMC3574439 | biostudies-literature | 2013 Jan

REPOSITORIES: biostudies-literature

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Ecological selection as the cause and sexual differentiation as the consequence of species divergence?

Oneal Elen E Knowles L Lacey LL

Proceedings. Biological sciences 20130101 1750

Key conceptual issues about speciation go unanswered without consideration of non-mutually exclusive factors. With tests based on speciation theory, we exploit the island distribution and habitat differences exhibited by the Caribbean cricket Amphiacusta sanctaecrucis, and with an analysis of divergent ecological selection, sexually selected differentiation and geographical isolation, address how these different factors interact. After testing for divergent selection by comparing neutral genetic ...[more]

PMID: 23173206

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Project description:Comparative genomics has contributed to the growing evidence that sexual selection is an important component of evolutionary divergence and speciation. Divergence by sexual selection is implicated in faster rates of divergence of the X chromosome and of genes thought to underlie sexually selected traits, including genes that are sex biased in expression. However, accurately inferring the relative importance of complex and interacting forms of natural selection, demography, and neutral processes that occurred in the evolutionary past is challenging. Experimental evolution provides an opportunity to apply controlled treatments for multiple generations and examine the consequent genomic divergence. Here, we altered sexual selection intensity, elevating sexual selection in polyandrous lines and eliminating it in monogamous lines, and examined patterns of allele frequency divergence in the genome of Drosophila pseudoobscura after more than 160 generations of experimental evolution. Divergence is not uniform across the genome but concentrated in "islands," many of which contain candidate genes implicated in mating behaviors and other sexually selected phenotypes. These are more often seen on the X chromosome, which also shows greater divergence in F ST than neutral expectations. There are characteristic signatures of selection seen in these regions, with lower diversity on the X chromosome than the autosomes, and differences in diversity on the autosomes between selection regimes. Reduced Tajima's D within some of the divergent regions may imply that selective sweeps have occurred, despite considerable recombination. These changes are associated with both differential gene expression between the lines and sex-biased gene expression within the lines. Our results are very similar to those thought to implicate sexual selection in divergence between species and natural populations, and hence provide experimental support for the likely role of sexual selection in driving such types of genetic divergence, but also illustrate how variable outcomes can be for different genomic regions.

Project description:Ecological speciation is a common mechanism by which new species arise. Despite great efforts, the role of gene expression in ecological divergence and speciation is poorly understood. Here, we conducted a genome-wide gene expression investigation of two Oryza species that are evolutionarily young and distinct in ecology and morphology. Using digital gene expression (DGE) technology and the paired-end RNA sequencing (RNA-Seq) method, we obtained 21,415 expressed genes across three reproduction-related tissues at two critical developmental stages. Of them, ~8% (1717) differed significantly in expression levels between the two species and these differentially expressed genes are randomly distributed across the genome. Moreover, 62% (1064) of the differentially expressed genes exhibited a signature of directional selection in at least one species. Importantly, the genes with differential expression between species evolved more rapidly at the 5â??flanking sequences than the genes without differential expression relative to coding sequences, suggesting that cis-regulatory changes are likely adaptive and play an important role in the ecological divergence of the two species. Finally, we showed evidence of significant differentiation between species in phenotype traits and observed that genes with differential expression were overrepresented with functional terms involving phenotypic and ecological differentiation between the two species, including reproduction- and stress-related characteristics. Our findings demonstrate that ecological speciation is associated with widespread and adaptive alterations in genome-wide gene expression and highlight the dominant role of regulatory evolution in ecological divergence and adaptation. We selected accessions representing typical Oryza rufipogon and O. nivara, which were sampled exclusively from South and Southeast Asia where the two species overlap. We chose to collect three types of tissues, i.e., flag leaves at the heading stage (2â??7 cm above the primary branch) (L), panicles at the heading stage (H) and panicles at the flowering stage (10â??15 cm above the primary branch) (F). Sample collection was repeated twice in two consecutive years (2009 and 2010) under the same controlled conditions. A total of 36 samples were sequenced by Illuminaâ??s digital gene expression (DGE) system, with each type of tissues collected from six individuals of each species as biological replicates. To access the quality of DGE technology, we also selected six samples representing three tissues from each of two individuals (one individual per species) for paired-end RNA-Seq sequencing.

Project description:BACKGROUND: Many species exhibit geographic variation in sexual signals, and divergence in these traits may lead to speciation. Sexual signals may diverge due to differences in ecology if the environment constrains signal production or transmission. Alternatively, sexual signals may diverge stochastically through sexual selection or genetic drift, with little environmental influence. To distinguish between these alternatives we quantified variation in two putative sexual signals--tail length and plumage color--and a suite of non-sexual morphometric traits across the geographic range of the red-backed fairy-wren (Malurus melanocephalus). We then tested for associations between these traits and a number of environmental variables using generalized dissimilarity models. RESULTS: Variation in morphometric traits was explained well by environmental variation, irrespective of geographic distance between sites. Among putative signals, variation in plumage color was best explained by geographic distance, whereas tail length was best explained by environmental variation. Divergence in male plumage color was not coincident with the boundary between genetic lineages, but was greatest across a contact zone located 300 km east of the genetic boundary. CONCLUSIONS: Morphometric traits describing size and shape have likely been subject to ecological selection and thus appear to track local environmental variation regardless of subspecies identity. Ecological selection appears to have also influenced the evolution of tail length as a signal, but has played a limited role in shaping geographic variation in plumage color, consistent with stochastic divergence in concert with Fisherian selection on this trait. The lack of coincidence between the genetic boundary and the contact zone between plumage types suggests that the sexual plumage signal of one subspecies has introgressed into the genetic background of the other. Thus, this study provides insight into the various ways in which signal evolution may occur within a species, and the geographic patterns of signal variation that can arise, especially following secondary contact.

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Ecological selection as the cause and sexual differentiation as the consequence of species divergence?

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Ecological selection as the cause and sexual differentiation as the consequence of species divergence?

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