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      Macroevolutionary diversification with limited niche disparity in a species-rich lineage of cold-climate lizards

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          Abstract

          Background

          Life diversifies via adaptive radiation when natural selection drives the evolution of ecologically distinct species mediated by their access to novel niche space, or via non-adaptive radiation when new species diversify while retaining ancestral niches. However, while cases of adaptive radiation are widely documented, examples of non-adaptively radiating lineages remain rarely observed. A prolific cold-climate lizard radiation from South America ( Phymaturus), sister to a hyper-diverse adaptive radiation ( Liolaemus), has extensively diversified phylogenetically and geographically, but with exceptionally minimal ecological and life-history diversification. This lineage, therefore, may offer unique opportunities to investigate the non-adaptive basis of diversification, and in combination with Liolaemus, to cover the whole spectrum of modes of diversification predicted by theory, from adaptive to non-adaptive. Using phylogenetic macroevolutionary modelling performed on a newly created 58-species molecular tree, we establish the tempo and mode of diversification in the Phymaturus radiation.

          Results

          Lineage accumulation in Phymaturus opposes a density-dependent (or ‘niche-filling’) process of diversification. Concurrently, we found that body size diversification is better described by an Ornstein-Uhlenbeck evolutionary model, suggesting stabilizing selection as the mechanism underlying niche conservatism (i.e., maintaining two fundamental size peaks), and which has predominantly evolved around two major adaptive peaks on a ‘Simpsonian’ adaptive landscape.

          Conclusions

          Lineage diversification of the Phymaturus genus does not conform to an adaptive radiation, as it is characterised by a constant rate of species accumulation during the clade’s history. Their strict habitat requirements (rocky outcrops), predominantly invariant herbivory, and especially the constant viviparous reproduction across species have likely limited their opportunities for adaptive diversifications throughout novel environments. This mode of diversification contrasts dramatically with its sister lineage Liolaemus, which geographically overlaps with Phymaturus, but exploits all possible microhabitats in these and other bioclimatic areas. Our study contributes importantly to consolidate these lizards (liolaemids) as promising model systems to investigate the entire spectrum of modes of species formations, from the adaptive to the non-adaptive extremes of the continuum.

          Electronic supplementary material

          The online version of this article (10.1186/s12862-018-1133-1) contains supplementary material, which is available to authorized users.

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          Most cited references71

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          Phylogenetic Comparative Analysis: A Modeling Approach for Adaptive Evolution

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            Ecological Speciation

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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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                Author and article information

                Contributors
                reaney.ashley@gmail.com
                monysalda@gmail.com
                DPincheiraDonoso@lincoln.ac.uk
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                6 February 2018
                6 February 2018
                2018
                : 18
                Affiliations
                [1 ]ISNI 0000 0004 0420 4262, GRID grid.36511.30, Laboratory of Evolutionary Ecology of Adaptations, School of Life Sciences, , University of Lincoln, Brayford Campus, ; Lincoln, Lincolnshire LN6 7DL UK
                [2 ]GRID grid.440625.1, Centro de Investigación en Recursos Naturales y Sustentabilidad, , Universidad Bernardo O’Higgins, ; Santiago, Chile
                [3 ]ISNI 0000 0001 2113 8111, GRID grid.7445.2, Department of Life Sciences, Imperial College London, Silwood Park Campus, ; Buckhurst Road, Ascot, Berkshire, SL5 7PY UK
                Article
                1133
                10.1186/s12862-018-1133-1
                5801843
                29409440
                b7bc9aba-1b77-41d4-ac0f-558477b82ba3
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                Categories
                Research Article
                Custom metadata
                © The Author(s) 2018

                Evolutionary Biology
                natural selection,non-adaptive radiation,diversification,niche conservatism,macroevolution,lizards,phymaturus

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