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Parallel evolution of gene expression between trophic specialists despite divergent genotypes and morphologies.

ABSTRACT: Parallel evolution of gene expression commonly underlies convergent niche specialization, but parallel changes in expression could also underlie divergent specialization. We investigated divergence in gene expression and whole-genome genetic variation across three sympatric Cyprinodon pupfishes endemic to San Salvador Island, Bahamas. This recent radiation consists of a generalist and two derived specialists adapted to novel niches: a scale-eating and a snail-eating pupfish. We sampled total mRNA from all three species at two early developmental stages and compared gene expression with whole-genome genetic differentiation among all three species in 42 resequenced genomes. Eighty percent of genes that were differentially expressed between snail-eaters and generalists were up or down regulated in the same direction between scale-eaters and generalists; however, there were no fixed variants shared between species underlying these parallel changes in expression. Genes showing parallel evolution of expression were enriched for effects on metabolic processes, whereas genes showing divergent expression were enriched for effects on cranial skeleton development and pigment biosynthesis, reflecting the most divergent phenotypes observed between specialist species. Our findings reveal that even divergent niche specialists may exhibit convergent adaptation to higher trophic levels through shared genetic pathways. This counterintuitive result suggests that parallel evolution in gene expression can accompany divergent ecological speciation during adaptive radiation.

SUBMITTER: McGirr JA

PROVIDER: S-EPMC6089502 | biostudies-literature | 2018 Apr

REPOSITORIES: biostudies-literature

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Parallel evolution of gene expression between trophic specialists despite divergent genotypes and morphologies.

McGirr Joseph A JA Martin Christopher H CH

Evolution letters 20180214 2

Parallel evolution of gene expression commonly underlies convergent niche specialization, but parallel changes in expression could also underlie divergent specialization. We investigated divergence in gene expression and whole-genome genetic variation across three sympatric <i>Cyprinodon</i> pupfishes endemic to San Salvador Island, Bahamas. This recent radiation consists of a generalist and two derived specialists adapted to novel niches: a scale-eating and a snail-eating pupfish. We sampled to ...[more]

PMID: 30283665

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Project description:Jumping is a rapid locomotory mode widespread in terrestrial organisms. However, it is a rare specialization in ants. Forward jumping has been reported within four distantly related ant genera: Gigantiops, Harpegnathos, Myrmecia, and Odontomachus. The temporal engagement of legs/body parts during jump, however, varies across these genera. It is unknown what morphological adaptations underlie such behaviors and whether jumping in ants is solely driven directly by muscle contraction or additionally relies on elastic recoil mechanism. We investigated the morphological adaptations for jumping behavior by comparing differences in the locomotory musculature between jumping and non-jumping relatives using X-ray micro-CT and 3D morphometrics. We found that the size-specific volumes of the trochanter depressor muscle (scm6) of the middle and hind legs are 3-5 times larger in jumping ants, and that one coxal remotor muscle (scm2) is reduced in volume in the middle and/or hind legs. Notably, the enlargement in the volume of other muscle groups is directly linked to the legs or body parts engaged during the jump. Furthermore, a direct comparison of the muscle architecture revealed two significant differences between jumping vs. non-jumping ants: First, the relative Physiological Cross-Sectional Area (PCSA) of the trochanter depressor muscles of all three legs were larger in jumping ants, except in the front legs of Odontomachus rixosus and Myrmecia nigrocincta; second, the relative muscle fiber length was shorter in jumping ants compared to non-jumping counterparts, except in the front legs of O. rixosus and M. nigrocincta. These results suggest that the difference in relative muscle volume in jumping ants is largely invested in the area (PCSA), and not in fiber length. There was no clear difference in the pennation angle between jumping and non-jumping ants. Additionally, we report that the hind leg length relative to body length was longer in jumping ants. Based on direct comparison of the observed vs. possible work and power output during jumps, we surmise that direct muscle contractions suffice to explain jumping performance in three species, except for O. rixosus, where the lack of data on jumping performance prevents us from drawing definitive conclusions for this particular species. We suggest that increased investment in jumping-relevant musculature is a primary morphological adaptation that separates jumping from non-jumping ants. These results elucidate the common and idiosyncratic morphological changes underlying this rare adaptation in ants. まとぅみ (Okinawan language-Uchinaaguchi) (Japanese) РЕЗЮМЕ (Kazakh) ZUSAMMENFASSUNG (German).

Dataset Information

Parallel evolution of gene expression between trophic specialists despite divergent genotypes and morphologies.

Publications

Parallel evolution of gene expression between trophic specialists despite divergent genotypes and morphologies.

Similar Datasets

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