Synopsis The concept of trade-offs permeates our thinking about adaptive evolution because they are exhibited at every level of biological organization, from molecular and cellular processes to organismal and ecological functions. Trade-offs inevitably arise because different traits do not occur in isolation, but instead are imbedded within complex, integrated systems that make up whole organisms. The genetic and mechanistic underpinning of trade-offs can be found in the pleiotropic nodes that occur in the biological pathways shared between traits. Yet, often trade-offs are only understood as statistical correlations, limiting the ability to evaluate the interplay between how selection and constraint interact during adaptive evolution. Here, we first review the classic paradigms in which physiologists and evolutionary biologists have studied trade-offs and highlight the ways in which network and molecular pathway approaches unify these paradigms. We discuss how these approaches allow researchers to evaluate why trade-offs arise and how selection can act to overcome trait correlations and evolutionary constraints. We argue that understanding how the conserved molecular pathways are shared between different traits and functions provides a conceptual framework for evolutionary biologists, physiologists, and molecular biologists to meaningfully work together toward the goal of understanding why correlations and trade-offs occur between traits. We briefly highlight the melanocortin system and the hormonal control of osmoregulation as two case studies where an understanding of shared molecular pathways reveals why trade-offs occur between seemingly unrelated traits. While we recognize that applying such approaches poses challenges and limitations particularly in the context of natural populations, we advocate for the view that focusing on the biological pathways responsible for trade-offs provides a unified conceptual context accessible to a broad range of integrative biologists.
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How to Investigate the Origins of Novelty: Insights Gained from Genetic, Behavioral, and Fitness Perspectives
Synopsis Biologists are drawn to the most extraordinary adaptations in the natural world, often referred to as evolutionary novelties, yet rarely do we understand the microevolutionary context underlying the origins of novel traits, behaviors, or ecological niches. Here we discuss insights gained into the origins of novelty from a research program spanning biological levels of organization from genotype to fitness in Caribbean pupfishes. We focus on a case study of the origins of novel trophic specialists on San Salvador Island, Bahamas and place this radiation in the context of other rapid radiations. We highlight questions that can be addressed about the origins of novelty at different biological levels, such as measuring the isolation of novel phenotypes on the fitness landscape, locating the spatial and temporal origins of adaptive variation contributing to novelty, detecting dysfunctional gene regulation due to adaptive divergence, and connecting behaviors with novel traits. Evolutionary novelties are rare, almost by definition, and we conclude that integrative case studies can provide insights into this rarity relative to the dynamics of adaptation to more common ecological niches and repeated parallel speciation, such as the relative isolation of novel phenotypes on fitness landscapes and the transient availability of ecological, genetic, and behavioral opportunities.
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- Award ID(s):
- 1938571
- NSF-PAR ID:
- 10414076
- Date Published:
- Journal Name:
- Integrative Organismal Biology
- Volume:
- 1
- Issue:
- 1
- ISSN:
- 2517-4843
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Adaptive radiations are characterized by the rapid proliferation of species. Explaining how adaptive radiations occur therefore depends, in part, on identifying how populations become reproductively isolated––and ultimately become different species. Such reproductive isolation could arise when populations adapting to novel niches experience selection to avoid interbreeding and, consequently, evolve mating traits that minimize such hybridization via the process of reinforcement. Here, we highlight that a downstream consequence of reinforcement is divergence of conspecific populations, and this further divergence can instigate species proliferation. Moreover, we evaluate when reinforcement will––and will not––promote species proliferation. Finally, we discuss empirical approaches to test what role, if any, reinforcement plays in species proliferation and, consequently, in adaptive radiation. To date, reinforcement’s downstream effects on species proliferation remain largely unknown and speculative. Because the ecological and evolutionary contexts in which adaptive radiations occur are conducive to reinforcement and its downstream consequences, adaptive radiations provide an ideal framework in which to evaluate reinforcement’s role in diversification.
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Abstract 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 (
GEM s), 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.GEM s 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 illustrateGEM s 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.GEM s 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 expectGEM s 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 makeGEM s much more than a modeling advance, but an important conceptual advance that bridges ecology and evolution through the central concept of heritable trait variation. -
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Synopsis “Sex” is often used to describe a suite of phenotypic and genotypic traits of an organism related to reproduction. However, these traits—gamete type, chromosomal inheritance, physiology, morphology, behavior, etc.—are not necessarily coupled, and the rhetorical collapse of variation into a single term elides much of the complexity inherent in sexual phenotypes. We argue that consideration of “sex” as a constructed category operating at multiple biological levels opens up new avenues for inquiry in our study of biological variation. We apply this framework to three case studies that illustrate the diversity of sex variation, from decoupling sexual phenotypes to the evolutionary and ecological consequences of intrasexual polymorphisms. We argue that instead of assuming binary sex in these systems, some may be better categorized as multivariate and nonbinary. Finally, we conduct a meta-analysis of terms used to describe diversity in sexual phenotypes in the scientific literature to highlight how a multivariate model of sex can clarify, rather than cloud, studies of sexual diversity within and across species. We argue that such an expanded framework of “sex” better equips us to understand evolutionary processes, and that as biologists, it is incumbent upon us to push back against misunderstandings of the biology of sexual phenotypes that enact harm on marginalized communities.
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Abstract Evolutionary change begins at the population scale. Therefore, understanding adaptive variation requires the identification of the factors maintaining and shaping standing genetic variation at the within‐population level. Spatial and temporal environmental heterogeneity represent ecological drivers of within‐population genetic variation, determining the evolutionary trajectory of populations along with random processes. Here, we focused on the effects of spatiotemporal heterogeneity on quantitative and molecular variation in a natural population of the annual plant Arabidopsis thaliana . We sampled 1093 individuals from a Spanish A. thaliana population across an area of 7.4 ha for 10 years (2012–2021). Based on a sample of 279 maternal lines, we estimated spatiotemporal variation in life‐history traits and fitness from a common garden experiment. We genotyped 884 individuals with nuclear microsatellites to estimate spatiotemporal variation in genetic diversity. We assessed spatial patterns by estimating spatial autocorrelation of traits and fine‐scale genetic structure. We analysed the relationships between phenotypic variation, geographical location and genetic relatedness, as well as the effects of environmental suitability and genetic rarity on phenotypic variation. The common garden experiment indicated that there was more temporal than spatial variation in life‐history traits and fitness. Despite the differences among years, genetic distance in ecologically relevant traits (e.g. flowering time) tended to be positively correlated to genetic distance among maternal lines, while isolation by distance was less important. Genetic diversity exhibited significant spatial structure at short distances, which were consistent among years. Finally, genetic rarity, and not environmental suitability, accounted for genetic variation in life‐history traits. Synthesis . Our study highlighted the importance of repeated sampling to detect the large amount of genetic diversity at the quantitative and molecular levels that a single A. thaliana population can harbour. Overall, population genetic attributes estimated from our long‐term monitoring scheme (genetic relatedness and genetic rarity), rather than biological (dispersal) or ecological (vegetation types and environmental suitability) factors, emerged as the most important drivers of within‐population structure of phenotypic variation in A. thaliana .more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/iob/obz018
