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Consequences of clonality for sexual fitness: Clonal expansion enhances fitness under spatially restricted dispersal.

ABSTRACT: Clonality is a pervasive feature of sessile organisms, but this form of asexual reproduction is thought to interfere with sexual fitness via the movement of gametes among the modules that comprise the clone. This within-clone movement of gametes is expected to reduce sexual fitness via mate limitation of male reproductive success and, in some cases, via the production of highly inbred (i.e., self-fertilized) offspring. However, clonality also results in the spatial expansion of the genetic individual (i.e., genet), and this should decrease distances gametes and sexually produced offspring must travel to avoid competing with other gametes and offspring from the same clone. The extent to which any negative effects of clonality on mating success might be offset by the positive effects of spatial expansion is poorly understood. Here, we develop spatially explicit models in which fitness was determined by the success of genets through their male and female sex functions. Our results indicate that clonality serves to increase sexual fitness when it is associated with the outward expansion of the genet. Our models further reveal that the main fitness benefit of clonal expansion might occur through the dispersal of offspring over a wider area compared with nonclonal phenotypes. We conclude that, instead of interfering with sexual reproduction, clonal expansion should often serve to enhance sexual fitness.

SUBMITTER: Van Drunen WE

PROVIDER: S-EPMC4517236 | biostudies-literature | 2015 Jul

REPOSITORIES: biostudies-literature

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Consequences of clonality for sexual fitness: Clonal expansion enhances fitness under spatially restricted dispersal.

Van Drunen Wendy E WE van Kleunen Mark M Dorken Marcel E ME

Proceedings of the National Academy of Sciences of the United States of America 20150720 29

Clonality is a pervasive feature of sessile organisms, but this form of asexual reproduction is thought to interfere with sexual fitness via the movement of gametes among the modules that comprise the clone. This within-clone movement of gametes is expected to reduce sexual fitness via mate limitation of male reproductive success and, in some cases, via the production of highly inbred (i.e., self-fertilized) offspring. However, clonality also results in the spatial expansion of the genetic indiv ...[more]

PMID: 26195748

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Project description:Clonality is a widespread life history trait in flowering plants that may be essential for population persistence, especially in environments where sexual reproduction is unpredictable. Frequent clonal reproduction, however, could hinder sexual reproduction by spatially aggregating ramets that compete with seedlings and reduce inter-genet pollination. Nevertheless, the role of clonality in relation to variable sexual reproduction in population dynamics is often overlooked. We combined population matrix models and pollination experiments to compare the demographic contributions of clonal and sexual reproduction in three Dicentra canadensis populations, one in a well-forested landscape and two in isolated forest remnants. We constructed stage-based transition matrices from 3 years of census data to evaluate annual population growth rates, λ. We used loop analysis to evaluate the relative contribution of different reproductive pathways to λ. Despite strong temporal and spatial variation in seed set, populations generally showed stable growth rates. Although we detected some pollen limitation of seed set, manipulative pollination treatments did not affect population growth rates. Clonal reproduction contributed significantly more than sexual reproduction to population growth in the forest remnants. Only at the well-forested site did sexual reproduction contribute as much as clonal reproduction to population growth. Flowering plants were more likely to transition to a smaller size class with reduced reproductive potential in the following year than similarly sized nonflowering plants, suggesting energy trade-offs between sexual and clonal reproduction at the individual level. Seed production had negligible effects on growth and tuber production of individual plants. Our results demonstrate that clonal reproduction is vital for population persistence in a system where sexual reproduction is unpredictable. The bias toward clonality may be driven by low fitness returns for resource investment in sexual reproduction at the individual level. However, chronic failure in sexual reproduction may exacerbate the imbalance between sexual and clonal reproduction and eventually lead to irreversible loss of sex in the population.

Project description:AimSpecies' ecological traits influence their spatial genetic patterns. Bedrock preference strongly shapes the phylogeography of alpine plants, but its interactions with other ecological traits have rarely been disentangled. Here, we explore whether dispersal ability and degree of habitat specialization account for divergent postglacial expansion patterns of high-elevation plants in spite of similar bedrock preference.LocationThe Pyrenees, southwestern Europe.TaxonCirsium glabrum (Asteraceae), Salix pyrenaica (Salicaceae) and Silene borderei (Caryophyllaceae).MethodsPhylogenetic, genetic structure and demographic modelling analyses based on restriction-site-associated DNA sequencing (RADseq) data from a range-wide populational sampling were conducted. Occurrence data and environmental variables were used to construct species distribution models, which were projected under current and Last Glacial Maximum conditions, and were combined with RADseq data to reconstruct the postglacial history of the study species. The degree of habitat specialization of each species was estimated based on the plant communities within which they occur, and their climatic niche breadth.ResultsSalix pyrenaica, which occupies a broad range of habitats, shows a high level of range filling, a blurred genetic structure and an admixture cline between the two main genetic groups, congruent with rapid postglacial expansion. The microsite specialists C. glabrum and S. borderei exhibit a strong genetic structure and low levels of range filling, indicative of slow postglacial expansion. The good disperser C. glabrum shows higher levels of admixture between genetic groups and weaker population differentiation than the poor disperser S. borderei.Main conclusionsFactors other than bedrock preference have a strong impact on the postglacial range dynamics of high-elevation species. Habitat specialization plays an important role, allowing species occupying a broad range of habitats to more rapidly expand their ranges after environmental change. The effect of dispersal ability is lower than expected for the study species.

Dataset Information

Consequences of clonality for sexual fitness: Clonal expansion enhances fitness under spatially restricted dispersal.

Publications

Consequences of clonality for sexual fitness: Clonal expansion enhances fitness under spatially restricted dispersal.

Similar Datasets

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