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Poecilogony, the production of both feeding (planktotrophic) and non-feeding (lecithotrophic) larvae, occurs in five species of sea slugs in clade Sacoglossa, but only two other animal species. Dispersive planktotrophic sea slugs have little genetic structure across the Caribbean or Indo-Pacific, but non-dispersive lecithotrophic species can be highly structured, with up to 80% of genetic covariance distributed among populations. However, exceptions include over-dispersed lecithotrophs (E. velutinus, E. subornata) and under-dispersed planktotrophs (E. pusilla). Here, we present three new cases of poecilogony: E. velutinus, E. subornata and E. papillosa were exclusively lecithotrophic in oligotrophic central Caribbean waters, but produced 90-100% planktotrophic clutches in higher productivity waters of coastal Panama. Larvae were cultured to metamorphosis in three weeks, and were genetically confirmed as conspecific to lecithotrophic egg-layers. Populations of E. velutinus and E. papillosa from coastal South America had higher genetic diversity and connectivity than in low-productivity sites, indicating local expression of planktotrophy as an explanation for anomalous population-genetic patterns. Conversely, E. pusilla was highly genetically structured across the Indo-Pacific; populations were highly divergent in mitochondrial DNA despite producing primarily planktotrophic larvae. Expression of eyespots at one week and early onset of downward swimming and crawling behavior typical of settling larvae suggest precompetent larvae of E. pusilla avoid advection from natal sites during planktonic development, increasing genetic isolation. Variable development and larval behavior may create unusual patterns of genetic population structure in tropical sea slugs. Quantifying larval behavior can ultimately improve oceanographic models and predictions of larval dispersal and connectivity to aid management and conservation efforts.
The intertidal marine snail Chlorostoma (formerly Tegula) funebralis has a wide geographic distribution, and across this range populations are exposed to large variations in temperature. Southern California (USA) populations generally occupy warmer climates and are presumably exposed to high air temperatures during low tides more often than northern California populations. C. funebralis' broad, thermally heterogeneous geographic range could promote local adaptation, or the fine-tuning of individuals to their local habitat via natural selection. However, this species also has pelagic larvae, and available genetic data have found no evidence for population structure, suggesting there may be extensive gene flow that could preclude local adaptation. Overall, the potential for adaptive differentiation in C. funebralis is unclear because the balance between selection for local adaptation and the rate of interpopulation gene flow is largely unknown. To address this issue phenotypic assays were used to identify initial evidence for local adaptation to heat stress in three northern and three southern California C. funebralis populations, and subsequently mRNA and DNA were sampled from these populations to examine transcriptome and genome-wide signatures of local adaptation. In the field, temperature data loggers were also deployed to explicitly quantify regional differences in thermal stress exposure among populations. The cumulative results of this work uncovered : (i) phenotypic evidence for local adaptation to heat stress between northern and southern California populations, with southern populations being more thermally tolerant than northern ones, (ii) region-specific transcriptomic responses to heat stress in northern and southern California, including unique gene expression strategies in southern populations that potentially confer higher thermal tolerance, (iii) differences in the frequency and magnitude of extreme thermal stress events in northern and southern California, and (iv) genomic evidence for ecological adaptation against a background of homogeneity in northern and southern California populations. Not only do these findings provide unique insights into region-specific responses of thermal stress response, but they also suggest that adaptation to local environmental differences can evolve despite a pelagic larval phase in C. funebralis. Accounting for intraspecific population variation in thermal tolerance may provide important insights for predicting how species distributions will respond to global warming.
Our understanding of evolution in marine ecosystems is framed by theories of speciation developed in terrestrial environments. In the ocean, however, speciation processes are likely to be different than on land. A general lack of absolute barriers, and the vast distances certain organisms can travel as larvae, mean that populations likely diverge in the presence of gene flow. The objective of this dissertation is to examine the relative contribution of different mechanisms of divergence in the sea in order to deepen our understanding of speciation. We examined the population genetics of ectoparasitic snails (Coralliophila radula, C. violacea) that specialize on Porites corals, and occupy a vast geographic and environmental range across the Indo-Pacific. In Chapter One, we used a comparative phylogeographic approach to explore whether populations of both taxa diverged across common geographic barriers, or due to adaptation to the host. We found striking evidence of genetic structure with geography for both snail species, and structure concordant with host within C. violacea populations. These findings suggest that in addition to historical sea level fluctuations, symbioses also contribute to diversification of these snails in the Coral Triangle. In Chapter Two, we used genome-wide data (SNPs) to investigate whether the ecological divergence we observed in C. violacea occurred via directional selection on different hosts and identify loci under selection. We saw genetic evidence of snail migration between hosts, as well as hybridization. By testing for FST outliers, we found loci under divergent selection, including a gene involved in the control of xenobiotic detoxification pathway gene expression, perhaps allowing snails to neutralize coral-specific toxins. These findings provide strong support for ecological divergence with gene flow, driven by adaptation to host. In Chapter Three, we focused on one ecomorph of C. violacea that inhabits coral reefs across a range of environmental conditions. Using genome-wide data and a global ocean-climate database, we identified signatures of geographic isolation and local adaptation. We saw four genetically distinct groups, consistent with results from Chapter One, with most divergence in peripheral populations. Searching for genetic associations with ocean climate variables, we found that the strongest driver of local adaptation was sea surface temperature variation. Our results show that local adaption to different environments likely reinforces neutral divergence, especially in peripheral populations.
These studies sometimes give conflicting results of how much variation is present within a population. One potential reason for differences in levels of nuclear variation and mitochondrial variation is due to differential dispersal rates and/or dispersal distances between the sexes. These ideas are explored through an analysis of data from the literature.
Our current knowledge of marine organisms and the factors affecting their ecology, distribution and evolution has been revolutionised by the use, in the last 20 years, of molecular population genetics tools. This book is the result of a meeting of world-leading experts, in Rio de Janeiro, where the state of the art of this field was reviewed. Topics covered include the molecular analysis of bio-invasions, the recent developments in marine biotechnology, the factors affecting levels of genetic variation and population structure in marine organisms and their application to conservation biology, fisheries and aquaculture. This is the first book dedicated to the genetic study of marine organisms. It will be very useful to biology students, scientists and anyone working or simply interested in areas such as marine biology, zoology, ecology, and population and molecular genetics.
"Not only is a wealth of evidence presented to support the model of punctuated equilibria, but Stanley's stream of refreshing insights into classic topics of evolution, such as living fossils, mass extinctions and adaptive radiations add further weight to the validity of the general model".--GEOLOGICAL MAGAZINE. "Overall, Stanley offers an imaginative treatment of almost every issue in macroevolution".--AMERICAN SCIENTIST. 192 illustrations.