Reproductive gene expression in a coral reef fish exposed to increasing temperature across generations.

Heather D Veilleux,Jennifer M Donelson

doi:10.1093/conphys/cox077

Abstract

Reproduction in marine fish is generally tightly linked with water temperature. Consequently, when adults are exposed to projected future ocean temperatures, reproductive output of many species declines precipitously. Recent research has shown that in the common reef fish, Acanthochromis polyacanthus, step-wise exposure to higher temperatures over two generations (parents: +1.5°C, offspring: +3.0°C) can improve reproductive output in the F2 generation compared to F2 fish that have experienced the same high temperatures over two generations (F1 parents: +3.0°C, F2 offspring: +3.0°C). To investigate how a step-wise increase in temperature between generations improved reproductive capacity, we tested the expression of well-known teleost reproductive genes in the brain and gonads of F2 fish using quantitative reverse transcription PCR and compared it among control (+0.0°C for two generations), developmental (+3.0°C in second generation only), step (+1.5°C in first generation and +3.0°C in second generation), and transgenerational (+3.0°C for two generations) treatments. We found that levels of gonadotropin receptor gene expression (Fshr and Lhcgr) in the testes were reduced in developmental and transgenerational temperature treatments, but were similar to control levels in the step treatment. This suggests Fshr and Lhcgr may be involved in regulating male reproductive capacity in A. polyacanthus. In addition, lower Fshb expression in the brain of females in all temperature treatments compared to control, suggests that Fshb expression, which is involved in vitellogenesis, is sensitive to high temperatures. Our results help elucidate key genes that facilitate successful reproduction in reef fishes when they experience a gradual increase in temperature across generations consistent with the trajectory of climate change.

Highlights

Climate change is predicted to raise tropical sea surface temperatures by as much as 3°C by 2100 (Collins et al, 2013) with profound implications for the function and productivity of marine ecosystems (Harley et al, 2006; Pörtner et al, 2014)
We found that levels of gonadotropin receptor gene expression (Fshr and Lhcgr) in the testes were reduced in developmental and transgenerational temperature treatments, but were similar to control levels in the step treatment
The reef fish A. polyacanthus can fully acclimate aerobic metabolism when both parents and offspring are exposed to the same elevated temperatures (Donelson et al, 2012; Veilleux et al, 2015), these fish were unable to reproduce at elevated temperatures; only when there was a more gradual increase in temperature over two generations did fish show improved reproductive capacity (Donelson et al, 2016)

Summary

Introduction

Climate change is predicted to raise tropical sea surface temperatures by as much as 3°C by 2100 (Collins et al, 2013) with profound implications for the function and productivity of marine ecosystems (Harley et al, 2006; Pörtner et al, 2014). Conditions could occur if a population has enough standing genetic variation (Munday et al, 2013), there is concern that for many species the time required for genetic evolution may exceed the rate of ocean warming (Parmesan, 2006). Beneficial acclimation occurs when physiological, morphological or behavioural phenotypes are plastically altered to better suit the environment (Angilletta, 2009). The phenotype of many animals can be adjusted in response to short-term changes in environmental conditions, such as daily or seasonal environmental fluctuations (reversible acclimation; Angilletta, 2009). Environmental conditions experienced during early ontogeny can induce phenotypic changes that persist throughout life (developmental plasticity) and parental exposure can alter the performance of their offspring in the same environment (transgenerational plasticity; Salinas et al, 2013; Torda et al, 2017)

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