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Microhabitat, microbiota, mitochondria and the epigenome shape the biparental legacy of heat exposure in a tropical arthropod
Ecology, Evolution and Conservation Biology
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As technology and policy advance towards sustainable energy sources, humanity is reaching a critical climax regarding climate change. Average global surface temperatures have risen by 1oC since pre-industrial levels, and it is estimated that temperatures will continue to rise by at least 1.5oC until at least 2100, despite mitigation efforts. The effect that such warming will have on biodiversity remains undetermined. Warming will likely have a substantial impact on tropical regions, which are a hotbed for biodiversity, and warming in tropical regions has already been associated with massive declines in species population numbers. Whether biodiversity will continue to decline, culminating in mass extinction, due to climate change depends on the ability of tropical species to adapt to new thermal limits. Tropical regions exhibit low seasonal variability, thus tropical species are adapted to little variation in environmental conditions and rapid increases in temperature may prove unsustainable for life. Tropical arthropods make up the majority of species in the tropics, with 1.3 million species described, and the true estimate at several million species. However, they are at especially high risk, since as ectotherms, arthropod metabolism increases exponentially with increases in ambient temperature. Understanding the effect of temperature on tropical arthropods is crucial to understanding biome dynamics to target conservation efforts as the planet continues to warm. Epigenetic mechanisms, or changes in gene expression without changes in the genetic sequence, provide a short-term plastic way for tropical arthropods to respond to climate change. Here,i I utilize a model ectothermic arthropod, Cordylochernes scorpioides, to investigate: (1) behavioral mechanisms for moderation of the effects of high temperature; (2) phenotypic, genetic and epigenetic effects of high temperature exposure on intergenerational inheritance, and (3) the microbial composition of individuals exposed to high temperature. This tropical arthropod has a unique reproductive biology, enabling non-invasive investigation into fitness effects and reproductive capacity, and it also exhibits high variation in the mitochondrial genome, which was exploited to determine how mitochondrial function may influence biological responses to climate change. In Chapter 1, I present the results of a study designed to determine how microclimate variation in lowland tropical rainforests impacts the abundance in C. scorpioides populations. Tropical rainforests exhibit high levels of fine-scale climatic variation, yet climate studies in these regions typically retrieve temperature data from large-scale weather stations. This provides an incomplete view of how tropical arthropods may experience temperature and change their behavior to compensate for warming. This species of arthropod inhabits decaying Ficus trees in their native Panamanian rainforests. Several Ficus trees occupied by C. scorpioides were found and microclimate variation was assessed by placing iButton temperature loggers in three types of microhabitat, frass, side/south, and top/north over two types of trees, fallen and standing, in open canopy or closed canopy habitats. C. scorpioides were then collected from the trees to estimate abundance. Reduced abundance was associated with the hottest microhabitats, top/north in open canopy trees, and high abundance was iiassociated with the coolest microhabitats, frass in closed canopy trees. Thus C. scorpioides actively manage exposure to high temperatures through behavioral mechanisms.In Chapter 2, I investigate whether phenotypes from simulated climate change can be passed to offspring intergenerationally. During nymphal development, C. scorpioides were placed in incubators programmed to diurnally fluctuate in correspondence with ambient temperature measurements from rainforest habitats found in Chapter 1. A split-brood design was employed where, upon birth, 40 pseudoscorpions were collected from each family and half were directly exposed to a control temperature regime and the other half to a high (+2.5o) temperature regime. Developmental, survival, and male and female reproductive traits were assayed. An intergenerational effects study was then carried to determine whether direct effects of high temperature exposure are transmitted to offspring maternally, paternally or through both sexes. Females and males directly exposed to the high temperature were mated to control males and females, respectively, to establish female outcross (FOUT) and male outcross (MOUT) families. Developmental, survival, and reproductive traits were then assayed on offspring. As in males directly exposed to high temperature, males with both high-temperature treated mothers and fathers had significantly reduced sperm counts, though this effect was stronger in males with high temperature mothers. Sperm counts were also significantly affected by haplotype, with A2 haplotype males producing the most sperm and B2 haplotype males the most negatively affected by high-temperature treatment of the parent. iiiFemale reproductive traits did not exhibit significant intergenerational effects, suggesting they are more robust to the effects of high temperature. However, high temperature effects on some non-reproductive traits, including reduced survivorship and reduced male offspring size, were transmitted maternally. Interestingly, although males born to high-temperature mothers exhibited reduced body size, their development time was not significantly reduced, as in the directly treated generation. By contrast, female offspring with high temperature fathers had reduced developmental time, but not significantly reduced body size, indicating an uncoupling of size-temperature dependence and developmental rate often associated with arthropod species. This is hypothesized to be due to C. scorpioides XX/XO system of sex determination, where epigenetic or genetic mutations acting on the males’ lone X chromosome make them more vulnerable to sex-linked effects of high temperature. However, males with high temperature mothers experienced some positive effects of reproduction, producing 22% more offspring than did males with control temperature mothers. The best explanation for this may be selection, where only the most genetically or epigenetically fit males were capable of siring offspring.In Chapter 3, I determined the potential for intergenerational epigenetic effects in males exposed to high temperature by assaying gene expression of protein-coding genes, transposable elements, and noncoding RNA of testicular and spermatic tissue. Transposable elements are mobile genetic elements able to excise themselves and move throughout the genome, capable of inducing genomic instability and disrupted gene expression, but they are typically ivcontrolled by epigenetic modifications to silence their expression. They are highly expressed in the germline, where suppression is achieved through targeted destruction by non-coding RNAs known as PIWI-interacting RNAs. Approximately 70% of the C. scorpioides genome consists of transposable elements/highly repetitive regions, an unusually high level for an arthropod species, making transposable element expression a likely factor in intergenerational inheritance of alternative phenotypes in males exposed to high temperature. Males exposed to high temperature were either dissected for removal of the testes or had their mating sequence interrupted to collect sperm, and RNA sequences annotated to determine levels of differential expression. Testicular protein-coding genes and transposable elements were significantly up- regulated, and testicular and spermatic piRNA expression were significantly down-regulated in males exposed to high temperature. Hence, high temperature exposure likely induces transposable element activity in the germline, and causes dysregulation of the epigenetic control mechanisms designed to silence them.Finally, in Chapter 4, I conducted microbial diversity analysis to determine whether other mechanisms may be responsible for alternative phenotypes intergenerationally inherited from exposure to high temperature. Diverse and healthy gut microbiomes play a key role in host metabolism, physiology, nutrition, immune function, and pathogen defense for many species, with differing microbial profiles associated with environmental factors, such as temperature and nutrition, and host factors, such as genotype or mitochondrial haplotype. On vthe other hand, dysbiosis, or imbalances in the gut microbiome, have been associated with a variety of diseases, including metabolic disorders, immune disorders, neurodegenerative disease, and psychological disorders. Growing evidence also suggests that crosstalk between the gut microbiome and the host is mediated by microbial-derived molecules that induce changes in the epigenetic mechanisms that regulate host gene expression. Microbial diversity of control temperature and high temperature C. scorpioides were analyzed using a factorial design of two temperature treatments and three haplotypes to investigate temperature, haplogroup, and interaction effects on the diversity and community composition of the C. scorpioides microbiome. Elevated temperature was associated with increased microbial diversity, which was a counterintuitive result as increased microbial diversity is often correlated with a healthy microbiome, yet elevated temperature induced maladaptive states in C. scorpioides. The most variation between microbial profiles was due to haplotype, with A1/A2 haplotypes having higher diversity than B2 haplotypes. Lack of appreciable temperature effects on the C. scorpioides microbiome coupled with significant haplogroup effects suggest that microbial composition changes are not responsible for detrimental phenotypic effects of a 2.5oC temperature increase found in Chapter 2, and that epigenetic mechanisms and loss of epigenetic control over transposable elements, as discovered in Chapter 3, are implicated instead.