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Evolutionary stasis of a heritable morphological trait in a wild fish population despite apparent directional selection.

ABSTRACT: Comparing observed versus theoretically expected evolutionary responses is important for our understanding of the evolutionary process, and for assessing how species may cope with anthropogenic change. Here, we document directional selection for larger female size in Atlantic salmon, using pedigree-derived estimates of lifetime reproductive success as a fitness measure. We show the trait is heritable and, thus, capable of responding to selection. The Breeder's Equation, which predicts microevolution as the product of phenotypic selection and heritability, predicted evolution of larger size. This was at odds, however, with the observed lack of either phenotypic or genetic temporal trends in body size, a so-called "paradox of stasis." To investigate this paradox, we estimated the additive genetic covariance between trait and fitness, which provides a prediction of evolutionary change according to Robertson's secondary theorem of selection (STS) that is unbiased by missing variables. The STS prediction was consistent with the observed stasis. Decomposition of phenotypic selection gradients into genetic and environmental components revealed a potential upward bias, implying unmeasured factors that covary with trait and fitness. These results showcase the power of pedigreed, wild population studies-which have largely been limited to birds and mammals-to study evolutionary processes on contemporary timescales.

SUBMITTER: O'Sullivan RJ

PROVIDER: S-EPMC6617767 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Evolutionary stasis of a heritable morphological trait in a wild fish population despite apparent directional selection.

O'Sullivan Ronan James RJ Aykanat Tutku T Johnston Susan E SE Kane Adam A Poole Russell R Rogan Ger G Prodöhl Paulo A PA Primmer Craig R CR McGinnity Philip P Reed Thomas Eric TE

Ecology and evolution 20190611 12

Comparing observed versus theoretically expected evolutionary responses is important for our understanding of the evolutionary process, and for assessing how species may cope with anthropogenic change. Here, we document directional selection for larger female size in Atlantic salmon, using pedigree-derived estimates of lifetime reproductive success as a fitness measure. We show the trait is heritable and, thus, capable of responding to selection. The Breeder's Equation, which predicts microevolu ...[more]

PMID: 31312431

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Project description:Heritable trait variation is a central and necessary ingredient of evolution. Trait variation also directly affects ecological processes, generating a clear link between evolutionary and ecological dynamics. Despite the changes in variation that occur through selection, drift, mutation, and recombination, current eco-evolutionary models usually fail to track how variation changes through time. Moreover, eco-evolutionary models assume fitness functions for each trait and each ecological context, which often do not have empirical validation. We introduce a new type of model, Gillespie eco-evolutionary models (GEMs), that resolves these concerns by tracking distributions of traits through time as eco-evolutionary dynamics progress. This is done by allowing change to be driven by the direct fitness consequences of model parameters within the context of the underlying ecological model, without having to assume a particular fitness function. GEMs work by adding a trait distribution component to the standard Gillespie algorithm - an approach that models stochastic systems in nature that are typically approximated through ordinary differential equations. We illustrate GEMs with the Rosenzweig-MacArthur consumer-resource model. We show not only how heritable trait variation fuels trait evolution and influences eco-evolutionary dynamics, but also how the erosion of variation through time may hinder eco-evolutionary dynamics in the long run. GEMs can be developed for any parameter in any ordinary differential equation model and, furthermore, can enable modeling of multiple interacting traits at the same time. We expect GEMs will open the door to a new direction in eco-evolutionary and evolutionary modeling by removing long-standing modeling barriers, simplifying the link between traits, fitness, and dynamics, and expanding eco-evolutionary treatment of a greater diversity of ecological interactions. These factors make GEMs much more than a modeling advance, but an important conceptual advance that bridges ecology and evolution through the central concept of heritable trait variation.

Project description:Background and aimsPatterns of morphological evolution at levels above family rank remain underexplored in the ferns. The present study seeks to address this gap through analysis of 79 morphological characters for 81 taxa, including representatives of all ten families of eupolypod II ferns. Recent molecular phylogenetic studies demonstrate that the evolution of the large eupolypod II clade (which includes nearly one-third of extant fern species) features unexpected patterns. The traditional 'athyrioid' ferns are scattered across the phylogeny despite their apparent morphological cohesiveness, and mixed among these seemingly conservative taxa are morphologically dissimilar groups that lack any obvious features uniting them with their relatives. Maximum-likelihood and maximum-parsimony character optimizations are used to determine characters that unite the seemingly disparate groups, and to test whether the polyphyly of the traditional athyrioid ferns is due to evolutionary stasis (symplesiomorphy) or convergent evolution. The major events in eupolypod II character evolution are reviewed, and character and character state concepts are reappraised, as a basis for further inquiries into fern morphology.MethodsCharacters were scored from the literature, live plants and herbarium specimens, and optimized using maximum-parsimony and maximum-likelihood, onto a highly supported topology derived from maximum-likelihood and Bayesian analysis of molecular data. Phylogenetic signal of characters were tested for using randomization methods and fitdiscrete.Key resultsThe majority of character state changes within the eupolypod II phylogeny occur at the family level or above. Relative branch lengths for the morphological data resemble those from molecular data and fit an ancient rapid radiation model (long branches subtended by very short backbone internodes), with few characters uniting the morphologically disparate clades. The traditional athyrioid ferns were circumscribed based upon a combination of symplesiomorphic and homoplastic characters. Petiole vasculature consisting of two bundles is ancestral for eupolypods II and a synapomorphy for eupolypods II under deltran optimization. Sori restricted to one side of the vein defines the recently recognized clade comprising Rhachidosoraceae through Aspleniaceae, and sori present on both sides of the vein is a synapomorphy for the Athyriaceae sensu stricto. The results indicate that a chromosome base number of x =41 is synapomorphic for all eupolypods, a clade that includes over two-thirds of extant fern species.ConclusionsThe integrated approach synthesizes morphological studies with current phylogenetic hypotheses and provides explicit statements of character evolution in the eupolypod II fern families. Strong character support is found for previously recognized clades, whereas few characters support previously unrecognized clades. Sorus position appears to be less complicated than previously hypothesized, and linear sori restricted to one side of the vein support the clade comprising Aspleniaceae, Diplaziopsidaceae, Hemidictyaceae and Rachidosoraceae - a lineage only recently identified. Despite x =41 being a frequent number among extant species, to our knowledge it has not previously been demonstrated as the ancestral state. This is the first synapomorphy proposed for the eupolypod clade, a lineage comprising 67 % of extant fern species. This study provides some of the first hypotheses of character evolution at the family level and above in light of recent phylogenetic results, and promotes further study in an area that remains open for original observation.

Dataset Information

Evolutionary stasis of a heritable morphological trait in a wild fish population despite apparent directional selection.

Publications

Evolutionary stasis of a heritable morphological trait in a wild fish population despite apparent directional selection.

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