Dataset Information

Reproductive plasticity of Hawaiian Montipora corals following thermal stress.

ABSTRACT: Ocean warming, fueled by climate change, is the primary cause of coral bleaching events which are predicted to increase in frequency. Bleaching is generally damaging to coral reproduction, can be exacerbated by concomitant stressors like ultraviolet radiation (UVR), and can have lasting impacts to successful reproduction and potential adaptation. We compared morphological and physiological reproductive metrics (e.g., sperm motility, mitochondrial membrane integrity, egg volume, gametes per bundle, and fertilization and settlement success) of two Hawaiian Montipora corals after consecutive bleaching events in 2014 and 2015. Between the species, sperm motility and mitochondrial membrane potential had the most disparate results. Percent sperm motility in M. capitata, which declined to ~ 40% during bleaching from a normal range of 70-90%, was still less than 50% motile in 2017 and 2018 and had not fully recovered in 2019 (63% motile). By contrast, percent sperm motility in Montipora spp. was 86% and 74% in 2018 and 2019, respectively. This reduction in motility was correlated with damage to mitochondria in M. capitata but not Montipora spp. A major difference between these species is the physiological foundation of their UVR protection, and we hypothesize that UVR protective mechanisms inherent in Montipora spp. mitigate this reproductive damage.

SUBMITTER: Henley EM

PROVIDER: S-EPMC8190081 | biostudies-literature | 2021 Jun

REPOSITORIES: biostudies-literature

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Reproductive plasticity of Hawaiian Montipora corals following thermal stress.

Henley E Michael EM Quinn Mariko M Bouwmeester Jessica J Daly Jonathan J Zuchowicz Nikolas N Lager Claire C Bailey Daniel W DW Hagedorn Mary M

Scientific reports 20210609 1

Ocean warming, fueled by climate change, is the primary cause of coral bleaching events which are predicted to increase in frequency. Bleaching is generally damaging to coral reproduction, can be exacerbated by concomitant stressors like ultraviolet radiation (UVR), and can have lasting impacts to successful reproduction and potential adaptation. We compared morphological and physiological reproductive metrics (e.g., sperm motility, mitochondrial membrane integrity, egg volume, gametes per bundl ...[more]

PMID: 34108494

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Project description:BackgroundEvolutionary patterns of scleractinian (stony) corals are difficult to infer given the existence of few diagnostic characters and pervasive phenotypic plasticity. A previous study of Hawaiian Montipora (Scleractinia: Acroporidae) based on five partial mitochondrial and two nuclear genes revealed the existence of a species complex, grouping one of the rarest known species (M. dilatata, which is listed as Endangered by the International Union for Conservation of Nature - IUCN) with widespread corals of very different colony growth forms (M. flabellata and M. cf. turgescens). These previous results could result from a lack of resolution due to a limited number of markers, compositional heterogeneity or reflect biological processes such as incomplete lineage sorting (ILS) or introgression.ResultsAll 13 mitochondrial protein-coding genes from 55 scleractinians (14 lineages from this study) were used to evaluate if a recent origin of the M. dilatata species complex or rate heterogeneity could be compromising phylogenetic inference. Rate heterogeneity detected in the mitochondrial data set seems to have no significant impacts on the phylogenies but clearly affects age estimates. Dating analyses show different estimations for the speciation of M. dilatata species complex depending on whether taking compositional heterogeneity into account (0.8 [0.05-2.6] Myr) or assuming rate homogeneity (0.4 [0.14-0.75] Myr). Genomic data also provided evidence of introgression among all analysed samples of the complex. RADseq data indicated that M. capitata colour morphs may have a genetic basis.ConclusionsDespite the volume of data (over 60,000 SNPs), phylogenetic relationships within the M. dilatata species complex remain unresolved most likely due to a recent origin and ongoing introgression. Species delimitation with genomic data is not concordant with the current taxonomy, which does not reflect the true diversity of this group. Nominal species within the complex are either undergoing a speciation process or represent ecomorphs exhibiting phenotypic polymorphisms.

Project description:BackgroundCorals, which form the foundation of biodiverse reef ecosystems, are under threat from warming oceans. Reefs provide essential ecological services, including food, income from tourism, nutrient cycling, waste removal, and the absorption of wave energy to mitigate erosion. Here, we studied the coral thermal stress response using network methods to analyze transcriptomic and polar metabolomic data generated from the Hawaiian rice coral Montipora capitata. Coral nubbins were exposed to ambient or thermal stress conditions over a 5-week period, coinciding with a mass spawning event of this species. The major goal of our study was to expand the inventory of thermal stress-related genes and metabolites present in M. capitata and to study gene-metabolite interactions. These interactions provide the foundation for functional or genetic analysis of key coral genes as well as provide potentially diagnostic markers of pre-bleaching stress. A secondary goal of our study was to analyze the accumulation of sex hormones prior to and during mass spawning to understand how thermal stress may impact reproductive success in M. capitata.MethodsM. capitata was exposed to thermal stress during its spawning cycle over the course of 5 weeks, during which time transcriptomic and polar metabolomic data were collected. We analyzed these data streams individually, and then integrated both data sets using MAGI (Metabolite Annotation and Gene Integration) to investigate molecular transitions and biochemical reactions.ResultsOur results reveal the complexity of the thermal stress phenome in M. capitata, which includes many genes involved in redox regulation, biomineralization, and reproduction. The size and number of modules in the gene co-expression networks expanded from the initial stress response to the onset of bleaching. The later stages involved the suppression of metabolite transport by the coral host, including a variety of sodium-coupled transporters and a putative ammonium transporter, possibly as a response to reduction in algal productivity. The gene-metabolite integration data suggest that thermal treatment results in the activation of animal redox stress pathways involved in quenching molecular oxygen to prevent an overabundance of reactive oxygen species. Lastly, evidence that thermal stress affects reproductive activity was provided by the downregulation of CYP-like genes and the irregular production of sex hormones during the mass spawning cycle. Overall, redox regulation and metabolite transport are key components of the coral animal thermal stress phenome. Mass spawning was highly attenuated under thermal stress, suggesting that global climate change may negatively impact reproductive behavior in this species.

Project description:Increasing temperature and thermal variability generate profound selection on populations. Given the fast rate of environmental change, understanding the role of plasticity and genetic adaptation in response to increasing temperatures is critical. This may be especially true for thermal effects on reproductive traits in which thermal fertility limits at high temperatures may be lower than for survival traits. Consequences of changing environments during development on adult phenotypes may be particularly problematic for core traits such as reproduction that begin early in development. Here we examine the consequences of developmental thermal plasticity on subsequent adult reproductive traits and its genetic basis. We used a panel of Drosophila melanogaster (the Drosophila Genetic Reference Panel; DGRP) in which male fertility performance was previously defined as either showing relatively little (status = 'high'-performing lines) or substantial ('low'-performing lines) decline when exposed to increasing developmental temperatures. We used a thermal reaction norm approach to quantify variation in the consequences of developmental thermal plasticity on multiple adult reproductive traits, including sex-specific responses, and to identify candidate genes underlying such variation. Developmental thermal stress impacted the means and thermal reaction norms of all reproductive traits except offspring sex ratio. Mating success declined as temperature increased with no difference between high and low lines, whereas increasing temperature resulted in declines for both male and female fertility and productivity but depended on line status. Fertility and offspring number were positively correlated within and between the sexes across lines, but males were more affected than females. We identified 933 SNPs with significant evolved genetic differentiation between high and low lines. In all, 54 of these lie within genomic windows of overall high differentiation, have significant effects of genotype on the male thermal reaction norm for productivity and are associated with 16 genes enriched for phenotypes affecting reproduction, stress responses and autophagy in Drosophila and other organisms. Our results illustrate considerable plasticity in male thermal limits on several reproductive traits following development at high temperature, and we identify differentiated loci with relevant phenotypic effects that may contribute to this population variation. While our work is on a single population, phenotypic results align with an increasing number of studies demonstrating the potential for stronger selection of thermal stress on reproductive traits, particularly in males. Such large fitness costs may have both short- and long-term consequences for the evolution of populations in response to a warming world.

Dataset Information

Reproductive plasticity of Hawaiian Montipora corals following thermal stress.

Publications

Reproductive plasticity of Hawaiian Montipora corals following thermal stress.

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