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Within-population covariation between sexual reproduction and susceptibility to local parasites.

ABSTRACT: Evolutionary biology has yet to reconcile the ubiquity of sex with its costs relative to asexual reproduction. Here, we test the hypothesis that coevolving parasites maintain sex in their hosts. Specifically, we examined the distributions of sexual reproduction and susceptibility to local parasites within a single population of freshwater snails (Potamopyrgus antipodarum). Susceptibility to local trematode parasites (Microphallus sp.) is a relative measure of the strength of coevolutionary selection in this system. Thus, if coevolving parasites maintain sex, sexual snails should be common where susceptibility is high. We tested this prediction in a mixed population of sexual and asexual snails by measuring the susceptibility of snails from multiple sites in a lake. Consistent with the prediction, the frequency of sexual snails was tightly and positively correlated with susceptibility to local parasites. Strikingly, in just two years, asexual females increased in frequency at sites where susceptibility declined. We also found that the frequency of sexual females covaries more strongly with susceptibility than with the prevalence of Microphallus infection in the field. In linking susceptibility to the frequency of sexual hosts, our results directly implicate spatial variation in coevolutionary selection in driving the geographic mosaic of sex.

SUBMITTER: Gibson AK

PROVIDER: S-EPMC5014691 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Within-population covariation between sexual reproduction and susceptibility to local parasites.

Gibson Amanda K AK Xu Julie Y JY Lively Curtis M CM

Evolution; international journal of organic evolution 20160727 9

Evolutionary biology has yet to reconcile the ubiquity of sex with its costs relative to asexual reproduction. Here, we test the hypothesis that coevolving parasites maintain sex in their hosts. Specifically, we examined the distributions of sexual reproduction and susceptibility to local parasites within a single population of freshwater snails (Potamopyrgus antipodarum). Susceptibility to local trematode parasites (Microphallus sp.) is a relative measure of the strength of coevolutionary selec ...[more]

PMID: 27402345

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Project description:Malaria parasites must undergo a round of sexual reproduction in the blood meal of a mosquito vector to be transmitted between hosts. Developing a transmission-blocking intervention to prevent parasites from mating is a major goal of biomedicine, but its effectiveness could be compromised if parasites can compensate by simply adjusting their sex allocation strategies. Recently, the application of evolutionary theory for sex allocation has been supported by experiments demonstrating that malaria parasites adjust their sex ratios in response to infection genetic diversity, precisely as predicted. Theory also predicts that parasites should adjust sex allocation in response to host immunity. Whilst data are supportive, the assumptions underlying this prediction - that host immune responses have differential effects on the mating ability of males and females - have not yet been tested. Here, we combine experimental work with theoretical models in order to investigate whether the development and fertility of male and female parasites is affected by innate immune factors and develop new theory to predict how parasites' sex allocation strategies should evolve in response to the observed effects. Specifically, we demonstrate that reactive nitrogen species impair gametogenesis of males only, but reduce the fertility of both male and female gametes. In contrast, tumour necrosis factor-? does not influence gametogenesis in either sex but impairs zygote development. Therefore, our experiments demonstrate that immune factors have complex effects on each sex, ranging from reducing the ability of gametocytes to develop into gametes, to affecting the viability of offspring. We incorporate these results into theory to predict how the evolutionary trajectories of parasite sex ratio strategies are shaped by sex differences in gamete production, fertility and offspring development. We show that medical interventions targeting offspring development are more likely to be 'evolution-proof' than interventions directed at killing males or females. Given the drive to develop medical interventions that interfere with parasite mating, our data and theoretical models have important implications.

Project description:Meiotic recombination of sex chromosomes is thought to be repressed in organisms with heterogametic sex determination (e.g. mammalian X/Y chromosomes), due to extensive divergence and chromosomal rearrangements between the two chromosomes. However, proper segregation of sex chromosomes during meiosis requires crossing-over occurring within the pseudoautosomal regions (PAR). Recent studies reveal that recombination, in the form of gene conversion, is widely distributed within and may have played important roles in the evolution of some chromosomal regions within which recombination was thought to be repressed, such as the centromere cores of maize. Cryptococcus neoformans, a major human pathogenic fungus, has an unusually large mating-type locus (MAT, >100 kb), and the MAT alleles from the two opposite mating-types show extensive nucleotide sequence divergence and chromosomal rearrangements, mirroring characteristics of sex chromosomes. Meiotic recombination was assumed to be repressed within the C. neoformans MAT locus. A previous study identified recombination hot spots flanking the C. neoformans MAT, and these hot spots are associated with high GC content. Here, we investigated a GC-rich intergenic region located within the MAT locus of C. neoformans to establish if this region also exhibits unique recombination behavior during meiosis. Population genetics analysis of natural C. neoformans isolates revealed signals of homogenization spanning this GC-rich intergenic region within different C. neoformans lineages, consistent with a model in which gene conversion of this region during meiosis prevents it from diversifying within each lineage. By analyzing meiotic progeny from laboratory crosses, we found that meiotic recombination (gene conversion) occurs around the GC-rich intergenic region at a frequency equal to or greater than the meiotic recombination frequency observed in other genomic regions. We discuss the implications of these findings with regards to the possible functional and evolutionary importance of gene conversion within the C. neoformans MAT locus and, more generally, in fungi.

Project description:Background and aimsIn dioecious plants, sexual reproduction requires close proximity to potential mates, but clonal growth can increase this distance and, therefore, reduce the probability of mating. Reduction in sexual propagules can lead to decreased dispersal and gene flow between populations. Gene flow and clonal growth may be further influenced by the size of the habitat patch. The effects of habitat size and reproductive mode (sexual or asexual reproduction) on spatial genetic structure and segregation of the sexes were tested by quantifying the distributions of genotypes and the sexes using the dioecious liverwort Marchantia inflexa.MethodsPlants were sampled from five pairs of small-large habitat patches to identify within- and among-population spatial genetic structure using 12 microsatellite markers. Spatial distributions were calculated as the likelihood that pairs of individuals were the same sex or genotype, and it was determined how that likelihood was affected by habitat patch size (small/large).Key resultsAsexual reproduction dominates within populations, and asexual dispersal also occurred across populations. Spatial segregation of the sexes was observed within populations; males were more likely to be near individuals of the same sex than were females. Although the likelihood of both sexes being near members of the same sex was similarly greater on small habitat patches, on large habitat patches male genotypes were almost 15 % more likely to be near clonemates than were female genotypes.ConclusionsThe results show a sex difference in clonal clumping that was dependent upon habitat size, suggesting differential colonization and/or survival between males and females. The sexes and genotypes being structured differently within and among populations have implications for the persistence of populations and the interactions between them. This study demonstrates that studying only the sexes and not their genotypes (or vice versa) can limit our understanding of the extent to which reproductive modes (sexual or asexual) influence genetic structure both within and between populations.

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Within-population covariation between sexual reproduction and susceptibility to local parasites.

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Within-population covariation between sexual reproduction and susceptibility to local parasites.

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