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      Body shape diversification along the benthic–pelagic axis in marine fishes

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          Abstract

          Colonization of novel habitats can result in marked phenotypic responses to the new environment that include changes in body shape and opportunities for further morphological diversification. Fishes have repeatedly transitioned along the benthic–pelagic axis, with varying degrees of association with the substrate. Previous work focusing on individual lineages shows that these transitions are accompanied by highly predictable changes in body form. Here, we generalize expectations drawn from this literature to study the effects of habitat on body shape diversification across 3344 marine teleost fishes. We compare rates and patterns of evolution in eight linear measurements of body shape among fishes that live in pelagic, demersal and benthic habitats. While average body shape differs between habitats, these differences are subtle compared with the high diversity of shapes found within each habitat. Benthic living increases the rate of body shape evolution and has led to numerous lineages evolving extreme body shapes, including both exceptionally wide bodies and highly elongate, eel-like forms. By contrast, we find that benthic living is associated with the slowest diversification of structures associated with feeding. Though we find that habitat can serve as an impetus for predictable trait changes, we also highlight the diversity of responses in marine teleosts to opportunities presented by major habitats.

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          Most cited references36

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          Adaptive radiation, ecological opportunity, and evolutionary determinism. American Society of Naturalists E. O. Wilson award address.

          Adaptive radiation refers to diversification from an ancestral species that produces descendants adapted to use a great variety of distinct ecological niches. In this review, I examine two aspects of adaptive radiation: first, that it results from ecological opportunity and, second, that it is deterministic in terms of its outcome and evolutionary trajectory. Ecological opportunity is usually a prerequisite for adaptive radiation, although in some cases, radiation can occur in the absence of preexisting opportunity. Nonetheless, many clades fail to radiate although seemingly in the presence of ecological opportunity; until methods are developed to identify and quantify ecological opportunity, the concept will have little predictive utility in understanding a priori when a clade might be expected to radiate. Although predicted by theory, replicated adaptive radiations occur only rarely, usually in closely related and poorly dispersing taxa found in the same region on islands or in lakes. Contingencies of a variety of types may usually preclude close similarity in the outcome of evolutionary diversification in other situations. Whether radiations usually unfold in the same general sequence is unclear because of the unreliability of methods requiring phylogenetic reconstruction of ancestral events. The synthesis of ecological, phylogenetic, experimental, and genomic advances promises to make the coming years a golden age for the study of adaptive radiation; natural history data, however, will always be crucial to understanding the forces shaping adaptation and evolutionary diversification.
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            Model inadequacy and mistaken inferences of trait-dependent speciation.

            Species richness varies widely across the tree of life, and there is great interest in identifying ecological, geographic, and other factors that affect rates of species proliferation. Recent methods for explicitly modeling the relationships among character states, speciation rates, and extinction rates on phylogenetic trees- BiSSE, QuaSSE, GeoSSE, and related models-have been widely used to test hypotheses about character state-dependent diversification rates. Here, we document the disconcerting ease with which neutral traits are inferred to have statistically significant associations with speciation rate. We first demonstrate this unfortunate effect for a known model assumption violation: shifts in speciation rate associated with a character not included in the model. We further show that for many empirical phylogenies, characters simulated in the absence of state-dependent diversification exhibit an even higher Type I error rate, indicating that the method is susceptible to additional, unknown model inadequacies. For traits that evolve slowly, the root cause appears to be a statistical framework that does not require replicated shifts in character state and diversification. However, spurious associations between character state and speciation rate arise even for traits that lack phylogenetic signal, suggesting that phylogenetic pseudoreplication alone cannot fully explain the problem. The surprising severity of this phenomenon suggests that many trait-diversification relationships reported in the literature may not be real. More generally, we highlight the need for diagnosing and understanding the consequences of model inadequacy in phylogenetic comparative methods.
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              Convergent evolution within an adaptive radiation of cichlid fishes.

              The recurrent evolution of convergent forms is a widespread phenomenon in adaptive radiations (e.g., [1-9]). For example, similar ecotypes of anoles lizards have evolved on different islands of the Caribbean, benthic-limnetic species pairs of stickleback fish emerged repeatedly in postglacial lakes, equivalent sets of spider ecomorphs have arisen on Hawaiian islands, and a whole set of convergent species pairs of cichlid fishes evolved in East African Lakes Malawi and Tanganyika. In all these cases, convergent phenotypes originated in geographic isolation from each other. Recent theoretical models, however, predict that convergence should be common within species-rich communities, such as species assemblages resulting from adaptive radiations. Here, we present the most extensive quantitative analysis to date of an adaptive radiation of cichlid fishes, discovering multiple instances of convergence in body and trophic morphology. Moreover, we show that convergent morphologies are associated with adaptations to specific habitats and resources and that Lake Tanganyika's cichlid communities are characterized by the sympatric occurrence of convergent forms. This prevalent coexistence of distantly related yet ecomorphologically similar species offers an explanation for the greatly elevated species numbers in cichlid species flocks. Copyright © 2012 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                Proceedings of the Royal Society B: Biological Sciences
                Proc. R. Soc. B.
                The Royal Society
                0962-8452
                1471-2954
                July 29 2020
                July 22 2020
                July 29 2020
                : 287
                : 1931
                : 20201053
                Affiliations
                [1 ]Department of Evolution and Ecology, University of California Davis, Davis, CA 95616, USA
                [2 ]Department of Biological Sciences, Clemson University, Clemson, SC 29634, USA
                Article
                10.1098/rspb.2020.1053
                32693721
                05b91469-7fd8-4e56-bcbe-5954fe1f4ddd
                © 2020

                https://royalsociety.org/-/media/journals/author/Licence-to-Publish-20062019-final.pdf

                https://royalsociety.org/journals/ethics-policies/data-sharing-mining/

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