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Gene expression correlates of social evolution in coral reef butterflyfishes.

ABSTRACT: Animals display remarkable variation in social behaviour. However, outside of rodents, little is known about the neural mechanisms of social variation, and whether they are shared across species and sexes, limiting our understanding of how sociality evolves. Using coral reef butterflyfishes, we examined gene expression correlates of social variation (i.e. pair bonding versus solitary living) within and between species and sexes. In several brain regions, we quantified gene expression of receptors important for social variation in mammals: oxytocin (OTR), arginine vasopressin (V1aR), dopamine (D1R, D2R) and mu-opioid (MOR). We found that social variation across individuals of the oval butterflyfish, Chaetodon lunulatus, is linked to differences in OTR,V1aR, D1R, D2R and MOR gene expression within several forebrain regions in a sexually dimorphic manner. However, this contrasted with social variation among six species representing a single evolutionary transition from pair-bonded to solitary living. Here, OTR expression within the supracommissural part of the ventral telencephalon was higher in pair-bonded than solitary species, specifically in males. These results contribute to the emerging idea that nonapeptide, dopamine and opioid signalling is a central theme to the evolution of sociality across individuals, although the precise mechanism may be flexible across sexes and species.

SUBMITTER: Nowicki JP

PROVIDER: S-EPMC7329040 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Gene expression correlates of social evolution in coral reef butterflyfishes.

Nowicki Jessica P JP Pratchett Morgan S MS Walker Stefan P W SPW Coker Darren J DJ O'Connell Lauren A LA

Proceedings. Biological sciences 20200624 1929

Animals display remarkable variation in social behaviour. However, outside of rodents, little is known about the neural mechanisms of social variation, and whether they are shared across species and sexes, limiting our understanding of how sociality evolves. Using coral reef butterflyfishes, we examined gene expression correlates of social variation (i.e. pair bonding versus solitary living) within and between species and sexes. In several brain regions, we quantified gene expression of receptor ...[more]

PMID: 32576103

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Project description:Coral reefs support diverse communities, and relationships among organisms within these communities are quite complex. Among the relationships, clarifying the habitat association and foraging substrate selection relative to habitat characteristics is of central importance to ecology since these two aspects are the fundamentals for survival and growth of organisms. The aims of the present study were to investigate the spatial distribution and feeding substrate selection of 14 species of butterflyfishes on an Okinawan coral reef in Japan. Species-specific spatial distributions varied with habitat characteristics (e.g., encrusting corals, massive corals, branching Acropora and rock). For feeding substrates, seven species of obligate coral polyp feeders exhibited significant positive selectivity for tabular Acropora, corymbose Acropora, encrusting corals and massive corals but significant negative selectivity for dead corals, coral rubble and rock. Among six species of facultative coral polyp feeders, two species exhibited significant positive selectivity for encrusting corals and massive corals, and one species showed significant positive selectivity for dead corals as feeding substrates. In contrast, three species exhibited no significant positive selectivity for any feeding substrates. A similar result was observed for one non-coralline invertebrate feeder. Among the 14 species, 12 species showed a relatively close relationship between spatial distribution and feeding substrates but the remaining two species did not. The present study is the first study to elucidate species-specific spatial distributions and feeding substrate selection of butterflyfishes on an Okinawan coral reef. The results of the present study suggest that diverse substrates, including various types of living corals (especially encrusting corals, massive corals, tabular Acropora, corymbose Acropora and branching Acropora) and non-coralline substrates (rock) are the primary determinants of spatial distributions and feeding sites. Thus, diverse substrates are important for maintaining high species diversity of butterflyfishes and changes of the substrates would likely change the spatial patterns and foraging behavior, although species-specific responses may be found, depending on their species-specific dependence on vulnerable substrates.

Project description:BackgroundUnderstanding the mechanisms by which natural populations cope with environmental stress is paramount to predict their persistence in the face of escalating anthropogenic impacts. Reef-building corals are increasingly exposed to local and global stressors that alter nutritional status causing reduced fitness and mortality, however, these responses can vary considerably across species and populations.Methodology/principal findingsWe compare the expression of 22 coral host genes in individuals from an inshore and an offshore reef location using quantitative Reverse Transcription-PCR (qRT-PCR) over the course of 26 days following translocation into a shaded, filtered seawater environment. Declines in lipid content and PSII activity of the algal endosymbionts (Symbiodinium ITS-1 type C2) over the course of the experiment indicated that heterotrophic uptake and photosynthesis were limited, creating nutritional deprivation conditions. Regulation of coral host genes involved in metabolism, CO2 transport and oxidative stress could be detected already after five days, whereas PSII activity took twice as long to respond. Opposing expression trajectories of Tgl, which releases fatty acids from the triacylglycerol storage, and Dgat1, which catalyses the formation of triglycerides, indicate that the decline in lipid content can be attributed, at least in part, by mobilisation of triacylglycerol stores. Corals from the inshore location had initially higher lipid content and showed consistently elevated expression levels of two genes involved in metabolism (aldehyde dehydrogenase) and calcification (carbonic anhydrase).Conclusions/significanceCoral host gene expression adjusts rapidly upon change in nutritional conditions, and therefore can serve as an early signature of imminent coral stress. Consistent gene expression differences between populations indicate that corals acclimatize and/or adapt to local environments. Our results set the stage for analysis of these processes in natural coral populations, to better understand the responses of coral communities to global climate change and to develop more efficient management strategies.

Dataset Information

Gene expression correlates of social evolution in coral reef butterflyfishes.

Publications

Gene expression correlates of social evolution in coral reef butterflyfishes.

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