BackgroundSex differences in the magnitude or direction of mutational effect may be important to a variety of population processes, shaping the mutation load and affecting the cost of sex itself. These differences are expected to be greatest after sexual maturity. Mutation-accumulation (MA) experiments provide the most direct way to examine the consequences of new mutations, but most studies have focused on juvenile viability without regard to sex, and on autosomes rather than sex chromosomes; both adult fitness and X-linkage have been little studied. We therefore investigated the effects of 50 generations of X-chromosome mutation accumulation on the fitness of males and females derived from an outbred population of Drosophila melanogaster.ResultsFitness declined rapidly in both sexes as a result of MA, but adult males showed markedly greater fitness loss relative to their controls compared to females expressing identical genotypes, even when females were made homozygous for the X. We estimate that these mutations are partially additive (h ~ 0.3) in females. In addition, the majority of new mutations appear to harm both males and females.ConclusionsOur data helps fill a gap in our understanding of the consequences of sexual selection for genetic load, and suggests that stronger selection on males may indeed purge deleterious mutations affecting female fitness.
Understanding the spatial scale of local adaptation and the factors associated with adaptive diversity are important objectives for ecology and evolutionary biology, and have significant implications for effective conservation and management of wild populations and natural resources. In this study, we used an environmental association analysis to identify important bioclimatic variables correlated with putatively adaptive genetic variation in a benthic marine invertebrate-the giant California sea cucumber (Parastichopus californicus)-spanning coastal British Columbia and southeastern Alaska. We used a redundancy analysis (RDA) with 3,699 single nucleotide polymorphisms (SNPs) obtained using RAD sequencing to detect candidate markers associated with 11 bioclimatic variables, including sea bottom and surface conditions, across two spatial scales (entire study area and within subregions). At the broadest scale, RDA revealed 59 candidate SNPs, 86% of which were associated with mean bottom temperature. Similar patterns were identified when population structure was accounted for. Additive polygenic scores, which provide a measure of the cumulative signal across all candidate SNPs, were strongly correlated with mean bottom temperature, consistent with spatially varying selection across a thermal gradient. At a finer scale, 23 candidate SNPs were detected, primarily associated with surface salinity (26%) and bottom current velocity (17%). Our findings suggest that environmental variables may play a role as drivers of spatially varying selection for P. californicus. These results provide context for future studies to evaluate the genetic basis of local adaptation in P. californicus and help inform the relevant scales and environmental variables for in situ field studies of putative adaptive variation in marine invertebrates. K E Y W O R D S climate data, environmental association analysis, marine invertebrate, RAD-sequencing, redundancy analysis, seascape genomics
The evolutionary theory of aging predicts that longevity will decline via drift or age-specific tradeoffs when selection favors early life fitness. Many Drosophila melanogaster populations continually terminated at young adult ages retain surprisingly long postselection lifespans. We compiled three decades of longevity data from the Ives population, demonstrating that postselective longevity was both substantial (30 days) and temporally stable over this period. Recently, alleles with positive pleiotropic effects between adjacent ages, particularly those affecting overall condition, have been integrated into the theory and may explain the extended longevity observed. We experimentally tested this hypothesis by isolating 20 hemiclones from Ives and allowing spontaneous mutations to accumulate (MA) for 35 generations. Fitness and longevity were positively genetically correlated in control females, and both traits declined due to MA. Crucially, MA induced a strong positive genetic correlation between the traits in both sexes, implying that mutations with early-life impacts also reduce late-life survival. Our results suggest that extended postreproductive longevity is actively maintained by selection for early-life fitness via positive pleiotropy and is not a merely a byproduct of exhaustion of genetic variation or weak drift. Thus mutation-selection balance for early fitness may govern variance in longevity in this system: a balance struck remarkably long after selection for continued survival ceases.
Adult reproductive success can account for a large fraction of male fitness, however, we know relatively little about the susceptibility of reproductive traits to mutation-accumulation (MA). Estimates of the mutational rate of decline for adult fitness and its components are controversial in Drosophila melanogaster, and post-copulatory performance has not been examined. We therefore separately measured the consequences of MA for total male reproductive success and its major pre-copulatory and post-copulatory components: mating success and sperm competitive success. We also measured juvenile viability, an important fitness component that has been well studied in MA experiments. MA had strongly deleterious effects on both male viability and adult fitness, but the latter declined at a much greater rate. Mutational pressure on total fitness is thus much greater than would be predicted by viability alone. We also noted a significant and positive correlation between all adult traits and viability in the MA lines, suggesting pleiotropy of mutational effect as required by 'good genes' models of sexual selection.
Life span differs between the sexes in many species. Three hypotheses to explain this interesting pattern have been proposed, involving different drivers: sexual selection, asymmetrical inheritance of cytoplasmic genomes, and hemizygosity of the X(Z) chromosome (the unguarded X hypothesis). Of these, the unguarded X has received the least experimental attention. This hypothesis suggests that the heterogametic sex suffers a shortened life span because recessive deleterious alleles on its single X(Z) chromosome are expressed unconditionally. In Drosophila melanogaster, the X chromosome is unusually large (∼20% of the genome), providing a powerful model for evaluating theories involving the X. Here, we test the unguarded X hypothesis by forcing D. melanogaster females from a laboratory population to express recessive X-linked alleles to the same degree as males, using females exclusively made homozygous for the X chromosome. We find no evidence for reduced life span or egg-to-adult viability due to X homozygozity. In contrast, males and females homozygous for an autosome both suffer similar, significant reductions in those traits. The logic of the unguarded X hypothesis is indisputable, but our results suggest that the degree to which recessive deleterious X-linked alleles depress performance in the heterogametic sex appears too small to explain general sex differences in life span.
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