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A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems.

ABSTRACT: A major goal of evolutionary science is to understand how biological diversity is generated and altered. Despite considerable advances, we still have limited insight into how phenotypic variation arises and is sorted by natural selection. Here we argue that an integrated view, which merges ecology, evolution and developmental biology (eco evo devo) on an equal footing, is needed to understand the multifaceted role of the environment in simultaneously determining the development of the phenotype and the nature of the selective environment, and how organisms in turn affect the environment through eco evo and eco devo feedbacks. To illustrate the usefulness of an integrated eco evo devo perspective, we connect it with the theory of resource polymorphism (i.e. the phenotypic and genetic diversification that occurs in response to variation in available resources). In so doing, we highlight fishes from recently glaciated freshwater systems as exceptionally well-suited model systems for testing predictions of an eco evo devo framework in studies of diversification. Studies on these fishes show that intraspecific diversity can evolve rapidly, and that this process is jointly facilitated by (i) the availability of diverse environments promoting divergent natural selection; (ii) dynamic developmental processes sensitive to environmental and genetic signals; and (iii) eco evo and eco devo feedbacks influencing the selective and developmental environments of the phenotype. We highlight empirical examples and present a conceptual model for the generation of resource polymorphism - emphasizing eco evo devo, and identify current gaps in knowledge.

SUBMITTER: Skulason S

PROVIDER: S-EPMC6852119 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems.

Skúlason Skúli S Parsons Kevin J KJ Svanbäck Richard R Räsänen Katja K Ferguson Moira M MM Adams Colin E CE Amundsen Per-Arne PA Bartels Pia P Bean Colin W CW Boughman Janette W JW Englund Göran G Guðbrandsson Jóhannes J Hooker Oliver E OE Hudson Alan G AG Kahilainen Kimmo K KK Knudsen Rune R Kristjánsson Bjarni K BK Leblanc Camille A-L CA Jónsson Zophonías Z Öhlund Gunnar G Smith Carl C Snorrason Sigurður S SS

Biological reviews of the Cambridge Philosophical Society 20190619 5

A major goal of evolutionary science is to understand how biological diversity is generated and altered. Despite considerable advances, we still have limited insight into how phenotypic variation arises and is sorted by natural selection. Here we argue that an integrated view, which merges ecology, evolution and developmental biology (eco evo devo) on an equal footing, is needed to understand the multifaceted role of the environment in simultaneously determining the development of the phenotype ...[more]

PMID: 31215138

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Project description:Eco-evolutionary dynamics result when interacting biological forces simultaneously produce demographic and genetic population responses. Eco-evolutionary simulators traditionally manage complexity by minimizing the influence of spatial pattern on process. However, such simplifications can limit their utility in real-world applications. We present a novel simulation modeling approach for investigating eco-evolutionary dynamics, centered on the driving role of landscape pattern. Our spatially-explicit, individual-based mechanistic simulation approach overcomes existing methodological challenges, generates new insights, and paves the way for future investigations in four focal disciplines: Landscape Genetics, Population Genetics, Conservation Biology, and Evolutionary Ecology. We developed a simple individual-based model to illustrate how spatial structure drives eco-evo dynamics. By making minor changes to our landscape's structure, we simulated continuous, isolated, and semi-connected landscapes, and simultaneously tested several classical assumptions of the focal disciplines. Our results exhibit expected patterns of isolation, drift, and extinction. By imposing landscape change on otherwise functionally-static eco-evolutionary models, we altered key emergent properties such as gene-flow and adaptive selection. We observed demo-genetic responses to these landscape manipulations, including changes in population size, probability of extinction, and allele frequencies. Our model also demonstrated how demo-genetic traits, including generation time and migration rate, can arise from a mechanistic model, rather than being specified a priori. We identify simplifying assumptions common to four focal disciplines, and illustrate how new insights might be developed in eco-evolutionary theory and applications by better linking biological processes to landscape patterns that we know influence them, but that have understandably been left out of many past modeling studies.

Project description:BackgroundUnderstanding how genes change during evolution to direct the development of diverse body plans is a major goal of the evo-devo field. Achieving this will require the establishment of new model systems that represent key points in phylogeny. These new model systems must be amenable to laboratory culture, and molecular and functional approaches should be feasible. To date, studies of insects have been best represented by the model system Drosophila melanogaster. Given the enormous diversity represented by insect taxa, comparative studies within this clade will provide a wealth of information about the evolutionary potential and trajectories of alternative developmental strategies.ResultsHere we established the beetle Dermestes maculatus, a member of the speciose clade Coleoptera, as a new insect model system. We have maintained a continuously breeding culture in the lab and documented Dermestes maculatus embryogenesis using nuclear and phalloidin staining. Anterior segments are specified during the blastoderm stage before gastrulation, and posterior segments are added sequentially during germ band elongation. We isolated and studied the expression and function of the pair-rule segmentation gene paired in Dermestes maculatus. In this species, paired is expressed in stripes during both blastoderm and germ band stages: four primary stripes arise prior to gastrulation, confirming an intermediate-germ mode of development for this species. As in other insects, these primary stripes then split into secondary stripes. To study gene function, we established both embryonic and parental RNAi. Knockdown of Dmac-paired with either method resulted in pair-rule-like segmentation defects, including loss of Engrailed expression in alternate stripes.ConclusionsThese studies establish basic approaches necessary to use Dermestes maculatus as a model system. Methods are now available for use of this intermediate-germ insect for future studies of the evolution of regulatory networks controlling insect segmentation, as well as of other processes in development and homeostasis. Consistent with the role of paired in long-germ Drosophila and shorter-germ Tribolium, paired functions as a pair-rule segmentation gene in Dermestes maculatus. Thus, paired retains pair-rule function in insects with different modes of segment addition.

Dataset Information

A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems.

Publications

A way forward with eco evo devo: an extended theory of resource polymorphism with postglacial fishes as model systems.

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