Dataset Information

Adaptive thermal plasticity enhances sperm and egg performance in a model insect.

ABSTRACT: Rising and more variable global temperatures pose a challenge for biodiversity, with reproduction and fertility being especially sensitive to heat. Here, we assessed the potential for thermal adaptation in sperm and egg function using Tribolium flour beetles, a warm-temperate-tropical insect model. Following temperature increases through adult development, we found opposing gamete responses, with males producing shorter sperm and females laying larger eggs. Importantly, this gamete phenotypic plasticity was adaptive: thermal translocation experiments showed that both sperm and eggs produced in warmer conditions had superior reproductive performance in warmer environments, and vice versa for cooler production conditions and reproductive environments. In warmer environments, gamete plasticity enabled males to double their reproductive success, and females could increase offspring production by one-third. Our results reveal exciting potential for sensitive but vital traits within reproduction to handle increasing and more variable thermal regimes in the natural environment.

SUBMITTER: Vasudeva R

PROVIDER: S-EPMC6773439 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Adaptive thermal plasticity enhances sperm and egg performance in a model insect.

Vasudeva Ramakrishnan R Sutter Andreas A Sales Kris K Dickinson Matthew E ME Lumley Alyson J AJ Gage Matthew Jg MJ

eLife 20191001

Rising and more variable global temperatures pose a challenge for biodiversity, with reproduction and fertility being especially sensitive to heat. Here, we assessed the potential for thermal adaptation in sperm and egg function using <i>Tribolium</i> flour beetles, a warm-temperate-tropical insect model. Following temperature increases through adult development, we found opposing gamete responses, with males producing shorter sperm and females laying larger eggs. Importantly, this gamete phenot ...[more]

PMID: 31570120

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Project description:The thermal biology of ectotherms is often used to infer species' responses to changes in temperature. It is often proposed that temperate species are more cold-tolerant, less heat-tolerant, more plastic, have broader thermal performance curves (TPCs) and lower optimal temperatures when compared to tropical species. However, relatively little empirical work has provided support for this using large interspecific studies. In the present study, we measure thermal tolerance limits and thermal performance in 22 species of Drosophila that developed under common conditions. Specifically, we measure thermal tolerance (CTmin and CTmax) as well as the fitness components viability, developmental speed and fecundity at seven temperatures to construct TPCs for each of these species. For 10 of the species, we also measure thermal tolerance and thermal performance following developmental acclimation to three additional temperatures. Using these data, we test several fundamental hypotheses about the evolution and plasticity of heat and cold resistance and thermal performance. We find that cold tolerance (CTmin) varied between the species according to the environmental temperature in the habitat from which they originated. These data support the idea that the evolution of cold tolerance has allowed species to persist in colder environments. However, contrary to expectation, we find that optimal temperature ( Topt) and the breadth of thermal performance ( Tbreadth) are similar in temperate, widespread and tropical species and we also find that the plasticity of TPCs was constrained. We suggest that the temperature range for optimal thermal performance is either fixed or under selection by the more similar temperatures that prevail during growing seasons. As a consequence, we find that Topt and Tbreadth are of limited value for predicting past, present and future distributions of species. This article is part of the theme issue 'Physiological diversity, biodiversity patterns and global climate change: testing key hypotheses involving temperature and oxygen'.

Project description:Fine-scale adaptive evolution is always constrained by strong gene flow at vertical level in marine organisms. Rapid environmental fluctuations and phenotypic plasticity through optimization of fitness-related traits in organisms play important roles in shaping intraspecific divergence. The coastal systems experience strong variations in multiple abiotic environmental factors, especially the temperature. We used a typical intertidal species, Pacific oyster (Crassostrea gigas), to investigate the interaction between plasticity and adaptive evolution. We collected intertidal and subtidal oysters from two ecological niches and carried out common garden experiments for one generation. We identified fine-scale vertical adaptive divergence between intertidal and subtidal F1 progeny at both sites, based on different hierarchical phenotypes, including morphological, physiological, and molecular traits. We further quantified the global plasticity to thermal stress through transcriptomic analysis. The intertidal oysters exhibited slow growth rate. However, they showed high survival and metabolic rates under heat stress, indicating vertically fine-scale phenotypic adaptive mechanisms and evolutionary trade-offs between growth and thermal tolerance. Transcriptomic analysis confirmed that the intertidal oysters have evolved high plasticity. The genes were classified into three types: evolutionarily divergent, concordantly plastic, and adaptive plastic genes. The evolved divergence between intertidal and subtidal oysters for these gene sets showed a significant positive correlation with plastic changes of subtidal populations in response to high temperature. Furthermore, the intertidal oysters exhibited delayed large-scale increase in expressional plasticity than that in subtidal counterparts. The same direction between plasticity and selection suggests that the oysters have evolved adaptive plasticity. This implies that adaptive plasticity facilitates the oyster to adapt to severe intertidal zones. The oysters exposed to strong environmental variability are thermal tolerant and have high adaptive potential to face the current global warming. Our findings will not only provide new insights into the significant role of plasticity in adaptive evolution that can be extended to other marine invertebrates, but also provide basic information for oyster resources conservation and reef reestablishment.

Dataset Information

Adaptive thermal plasticity enhances sperm and egg performance in a model insect.

Publications

Adaptive thermal plasticity enhances sperm and egg performance in a model insect.

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