Genome-wide analysis of genetic load and larval mortality in a highly fecund marine invertebrate, the Pacific Oyster Crassostrea gigas

Most marine fish and shellfish are very fecund, with females often producing many millions of eggs per spawn (Thorson 1950, Winemiller and Rose 1992). Their larval offspring characteristically suffer high (type-III) mortality, while developing for days to weeks in the plankton, but this mortality is...

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Bibliographic Details
Main Author: Plough, Louis Valentine
Format: Dataset
Language:English
Published: University of Southern California Digital Library (USC.DL) 2015
Subjects:
Online Access:https://dx.doi.org/10.25549/usctheses-c127-660319
http://digitallibrary.usc.edu/cdm/ref/collection/p15799coll127/id/660319
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Summary:Most marine fish and shellfish are very fecund, with females often producing many millions of eggs per spawn (Thorson 1950, Winemiller and Rose 1992). Their larval offspring characteristically suffer high (type-III) mortality, while developing for days to weeks in the plankton, but this mortality is largely attributed by most marine scientists to environmental factors. The biological and ecological characteristics of this life history mode have profound implications for population structure, adaptation, and recruitment variation, yet relatively little is known about the role of endogenous variation during the early life stages. Experimental inbred crosses of the highly fecund Pacific oyster Crassostrea gigas have previously revealed a high genetic load, which causes substantial genotype-dependent mortality, explains widespread observations of segregation distortion in crosses of other highly fecund marine bivalves, and fits predictions (Williams 1975) that high fecundity species should suffer substantial inbreeding depression (Launey and Hedgecock 2001, Bucklin 2003). Though these previous studies provided important experimental verification of high genetic load in the oyster, they left unanswered a number of questions about the genetic basis of this load and whether it could explain the high, early life-history mortality observed in the oyster. These questions can now be addressed, thanks to the advent of genome-wide statistical approaches, such as quantitative-trait locus (QTL) mapping. In this dissertation, a series of experiments were performed to address these and other questions, by creating experimental inbred and outbred families and analyzing molecular marker segregation data across the genome to detect the number, location, and effect of deleterious mutations in the Pacific oyster. There were four major findings. First, inbred families exhibited 10-15, mainly recessive or partially dominant, deleterious mutations, with little evidence for epistatic interaction between them. Genotype-dependent mortality calculated from the multiplicative fitness effects of these deleterious loci was ~96%, accounting for nearly all observed actual mortality. Second, the expression of genetic load occurred primarily during the larval stages in inbred crosses, with half of all deleterious mutations expressed during settlement and metamorphosis; further analysis revealed that mutations expressed at metamorphosis occurred over a relatively small temporal window, just prior to and during metamorphosis, but not after. Third, the environment significantly affected the fitness of deleterious alleles; dominance of and selection against some deleterious alleles increased significantly in a stressful, nutrient-deficient algal diet, while other alleles were un-affected, suggesting that inbreeding depression is caused by different loci in different environments. Fourth, seven to nine deleterious mutations were detected in wild families, causing an estimated 87-98% cumulative genetic mortality. Overall, there appears to be remarkable genetic variation in viability during the early life-stages of the Pacific oyster, causing much of the mortality that is observed in wild and inbred cultures. These results suggest that larvae of highly fecund marine animals in the natural environment may also be subject to substantial genotype-dependent mortality, which possibly contributes to the high recruitment variation and fluctuations in abundance of fished populations. The results of the dissertation also have broad implications for understanding the genetic basis of inbreeding depression, conservation genetics, and shellfish aquaculture.