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Cryptic fitness advantage: diploids invade haploid populations despite lacking any apparent advantage as measured by standard fitness assays.

ABSTRACT: Ploidy varies tremendously within and between species, yet the factors that influence when or why ploidy variants are adaptive remains poorly understood. Our previous work found that diploid individuals repeatedly arose within ten replicate haploid populations of Saccharomyces cerevisiae, and in each case we witnessed diploid takeover within ~1800 asexual generations of batch culture evolution in the lab. The character that allowed diploids to rise in frequency within haploid populations remains unknown. Here we present a number of experiments conducted with the goal to determine what this trait (or traits) might have been. Experiments were conducted both by sampling a small number of colonies from the stocks frozen every two weeks (~ 93 generations) during the original experiment, as well through sampling a larger number of colonies at the two time points where polymorphism for ploidy was most prevalent. Surprisingly, none of our fitness component measures (lag phase, growth rate, biomass production) indicated an advantage to diploidy. Similarly, competition assays against a common competitor and direct competition between haploid and diploid colonies isolated from the same time point failed to indicate a diploid advantage. Furthermore, we uncovered a tremendous amount of trait variation among colonies of the same ploidy level. Only late-appearing diploids showed a competitive advantage over haploids, indicating that the fitness advantage that allowed eventual takeover was not diploidy per se but an attribute of a subset of diploid lineages. Nevertheless, the initial rise in diploids to intermediate frequency cannot be explained by any of the fitness measures used; we suggest that the resolution to this mystery is negative frequency-dependent selection, which is ignored in the standard fitness measures used.

SUBMITTER: Gerstein AC

PROVIDER: S-EPMC3235103 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Cryptic fitness advantage: diploids invade haploid populations despite lacking any apparent advantage as measured by standard fitness assays.

Gerstein Aleeza C AC Otto Sarah P SP

PloS one 20111209 12

Ploidy varies tremendously within and between species, yet the factors that influence when or why ploidy variants are adaptive remains poorly understood. Our previous work found that diploid individuals repeatedly arose within ten replicate haploid populations of Saccharomyces cerevisiae, and in each case we witnessed diploid takeover within ~1800 asexual generations of batch culture evolution in the lab. The character that allowed diploids to rise in frequency within haploid populations remains ...[more]

PMID: 22174734

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Project description:Previous studies document a mental health advantage in British Indian children, particularly for externalising problems. The causes of this advantage are unknown.Subjects were 13,836 White children and 361 Indian children aged 5-16 years from the English subsample of the British Child and Adolescent Mental Health Surveys. The primary mental health outcome was the parent Strengths and Difficulties Questionnaire (SDQ). Mental health was also assessed using the teacher and child SDQs; diagnostic interviews with parents, teachers and children; and multi-informant clinician-rated diagnoses. Multiple child, family, school and area factors were examined as possible mediators or confounders in explaining observed ethnic differences.Indian children had a large advantage for externalising problems and disorders, and little or no difference for internalising problems and disorders. This was observed across all mental health outcomes, including teacher-reported and diagnostic interview measures. Detailed psychometric analyses provided no suggestion of information bias. The Indian advantage for externalising problems was partly mediated by Indian children being more likely to live in two-parent families and less likely to have academic difficulties. Yet after adjusting for these and all other covariates, the unexplained Indian advantage only reduced by about a quarter (from 1.08 to .71 parent SDQ points) and remained highly significant (p < .001). This Indian advantage was largely confined to families of low socio-economic position.The Indian mental health advantage is real and is specific to externalising problems. Family type and academic abilities mediate part of the advantage, but most is not explained by major risk factors. Likewise unexplained is the absence in Indian children of a socio-economic gradient in mental health. Further investigation of the Indian advantage may yield insights into novel ways to promote child mental health and child mental health equity in all ethnic groups.

Project description:To date, research on the evolution of sex chromosomes has focused on sexually antagonistic selection among diploids, which has been shown to be a potent driver of the strata and reduced recombination that characterize many sex chromosomes. However, significant selection can also occur on haploid genotypes during less conspicuous life cycle stages, e.g., competition among sperm/pollen or meiotic drive during gamete/spore production. These haploid selective processes are typically sex-specific, e.g., gametic/gametophytic competition typically occurs among sperm/pollen, and meiotic drive typically occurs during either spermatogenesis or oogenesis. We use models to investigate whether sex-specific selection on haploids could drive the evolution of recombination suppression on the sex chromosomes, as has been demonstrated for sex-specific selection among diploids. A potential complication is that zygotic sex-ratios become biased when haploid selected loci become linked to the sex-determining region because the zygotic sex ratio is determined by the relative number and fitness of X- vs. Y-bearing sperm. Despite causing biased zygotic sex-ratios, we find that a period of sex-specific haploid selection generally favors recombination suppression on the sex chromosomes. Suppressed recombination is favored because it allows associations to build up between haploid-beneficial alleles and the sex that experiences haploid selection most often (e.g., pollen beneficial alleles become strongly associated with the male determining region, Y or Z). Haploid selected loci can favor recombination suppression even in the absence of selective differences between male and female diploids. Overall, we expand our view of the sex-specific life cycle stages that can drive sex chromosome evolution to include gametic competition and meiotic drive. Based on our models, sex chromosomes should become enriched for genes that experience haploid selection, as is expected for genes that experience sexually antagonistic selection. Thus, we generate a number of predictions that can be evaluated in emerging sex chromosome systems.

Project description:BACKGROUND:Understanding genomic and phenotypic diversity among cryptic pest taxa has important implications for the management of pests and diseases. The diamondback moth, Plutella xylostella L., has been intensively studied due to its ability to evolve insecticide resistance and status as the world's most destructive pest of brassicaceous crops. The surprise discovery of a cryptic species endemic to Australia, Plutella australiana Landry & Hebert, raised questions regarding the distribution, ecological traits and pest status of the two species, the capacity for gene flow and whether specific management was required. Here, we collected Plutella from wild and cultivated brassicaceous plants from 75 locations throughout Australia and screened 1447 individuals to identify mtDNA lineages and Wolbachia infections. We genotyped genome-wide SNP markers using RADseq in coexisting populations of each species. In addition, we assessed reproductive compatibility in crossing experiments and insecticide susceptibility phenotypes using bioassays. RESULTS:The two Plutella species coexisted on wild brassicas and canola crops, but only 10% of Plutella individuals were P. australiana. This species was not found on commercial Brassica vegetable crops, which are routinely sprayed with insecticides. Bioassays found that P. australiana was 19-306 fold more susceptible to four commonly-used insecticides than P. xylostella. Laboratory crosses revealed that reproductive isolation was incomplete but directionally asymmetric between the species. However, genome-wide nuclear SNPs revealed striking differences in genetic diversity and strong population structure between coexisting wild populations of each species. Nuclear diversity was 1.5-fold higher in P. australiana, yet both species showed limited variation in mtDNA. Infection with a single Wolbachia subgroup B strain was fixed in P. australiana, suggesting that a selective sweep contributed to low mtDNA diversity, while a subgroup A strain infected just 1.5% of P. xylostella. CONCLUSIONS:Despite sympatric distributions and the capacity to hybridize, strong genomic and phenotypic divergence exists between these Plutella species that is consistent with contrasting colonization histories and reproductive isolation after secondary contact. Although P. australiana is a potential pest of brassicaceous crops, it is of secondary importance to P. xylostella.

Dataset Information

Cryptic fitness advantage: diploids invade haploid populations despite lacking any apparent advantage as measured by standard fitness assays.

Publications

Cryptic fitness advantage: diploids invade haploid populations despite lacking any apparent advantage as measured by standard fitness assays.

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