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      Cretaceous environmental changes led to high extinction rates in a hyperdiverse beetle family

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          Abstract

          Background

          As attested by the fossil record, Cretaceous environmental changes have significantly impacted the diversification dynamics of several groups of organisms. A major biome turnover that occurred during this period was the rise of angiosperms starting ca. 125 million years ago. Though there is evidence that the latter promoted the diversification of phytophagous insects, the response of other insect groups to Cretaceous environmental changes is still largely unknown. To gain novel insights on this issue, we assess the diversification dynamics of a hyperdiverse family of detritivorous beetles (Tenebrionidae) using molecular dating and diversification analyses.

          Results

          Age estimates reveal an origin after the Triassic-Jurassic mass extinction (older than previously thought), followed by the diversification of major lineages during Pangaean and Gondwanan breakups. Dating analyses indicate that arid-adapted species diversified early, while most of the lineages that are adapted to more humid conditions diversified much later. Contrary to other insect groups, we found no support for a positive shift in diversification rates during the Cretaceous; instead there is evidence for an 8.5-fold increase in extinction rates that was not compensated by a joint increase in speciation rates.

          Conclusions

          We hypothesize that this pattern is better explained by the concomitant reduction of arid environments starting in the mid-Cretaceous, which likely negatively impacted the diversification of arid-adapted species that were predominant at that time.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12862-014-0220-1) contains supplementary material, which is available to authorized users.

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          Most cited references54

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          Ecological and Evolutionary Responses to Recent Climate Change

          Ecological changes in the phenology and distribution of plants and animals are occurring in all well-studied marine, freshwater, and terrestrial groups. These observed changes are heavily biased in the directions predicted from global warming and have been linked to local or regional climate change through correlations between climate and biological variation, field and laboratory experiments, and physiological research. Range-restricted species, particularly polar and mountaintop species, show severe range contractions and have been the first groups in which entire species have gone extinct due to recent climate change. Tropical coral reefs and amphibians have been most negatively affected. Predator-prey and plant-insect interactions have been disrupted when interacting species have responded differently to warming. Evolutionary adaptations to warmer conditions have occurred in the interiors of species' ranges, and resource use and dispersal have evolved rapidly at expanding range margins. Observed genetic shifts modulate local effects of climate change, but there is little evidence that they will mitigate negative effects at the species level.
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            A comprehensive phylogeny of beetles reveals the evolutionary origins of a superradiation.

            Beetles represent almost one-fourth of all described species, and knowledge about their relationships and evolution adds to our understanding of biodiversity. We performed a comprehensive phylogenetic analysis of Coleoptera inferred from three genes and nearly 1900 species, representing more than 80% of the world's recognized beetle families. We defined basal relationships in the Polyphaga supergroup, which contains over 300,000 species, and established five families as the earliest branching lineages. By dating the phylogeny, we found that the success of beetles is explained neither by exceptional net diversification rates nor by a predominant role of herbivory and the Cretaceous rise of angiosperms. Instead, the pre-Cretaceous origin of more than 100 present-day lineages suggests that beetle species richness is due to high survival of lineages and sustained diversification in a variety of niches.
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              Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds.

              We implement a Bayesian Markov chain Monte Carlo algorithm for estimating species divergence times that uses heterogeneous data from multiple gene loci and accommodates multiple fossil calibration nodes. A birth-death process with species sampling is used to specify a prior for divergence times, which allows easy assessment of the effects of that prior on posterior time estimates. We propose a new approach for specifying calibration points on the phylogeny, which allows the use of arbitrary and flexible statistical distributions to describe uncertainties in fossil dates. In particular, we use soft bounds, so that the probability that the true divergence time is outside the bounds is small but nonzero. A strict molecular clock is assumed in the current implementation, although this assumption may be relaxed. We apply our new algorithm to two data sets concerning divergences of several primate species, to examine the effects of the substitution model and of the prior for divergence times on Bayesian time estimation. We also conduct computer simulation to examine the differences between soft and hard bounds. We demonstrate that divergence time estimation is intrinsically hampered by uncertainties in fossil calibrations, and the error in Bayesian time estimates will not go to zero with increased amounts of sequence data. Our analyses of both real and simulated data demonstrate potentially large differences between divergence time estimates obtained using soft versus hard bounds and a general superiority of soft bounds. Our main findings are as follows. (1) When the fossils are consistent with each other and with the molecular data, and the posterior time estimates are well within the prior bounds, soft and hard bounds produce similar results. (2) When the fossils are in conflict with each other or with the molecules, soft and hard bounds behave very differently; soft bounds allow sequence data to correct poor calibrations, while poor hard bounds are impossible to overcome by any amount of data. (3) Soft bounds eliminate the need for "safe" but unrealistically high upper bounds, which may bias posterior time estimates. (4) Soft bounds allow more reliable assessment of estimation errors, while hard bounds generate misleadingly high precisions when fossils and molecules are in conflict.
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                Author and article information

                Contributors
                kergoat@supagro.inra.fr
                Patrice.Bouchard@agr.gc.ca
                Anne-Laure.Clamens@supagro.inra.fr
                jessie.abbate@gmail.com
                herve.jourdan@ird.fr
                Roula.Zahab@cefe.cnrs.fr
                genson@supagro.inra.fr
                soldati@supagro.inra.fr
                fabien.condamine@gmail.com
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                21 October 2014
                21 October 2014
                2014
                : 14
                : 1
                : 220
                Affiliations
                [ ]INRA - UMR 1062 CBGP (INRA, IRD, CIRAD, Montpellier SupAgro), Campus de Baillarguet, 34988 Montferrier-sur-Lez, France
                [ ]Canadian National Collection of Insects, Arachnids and Nematodes, Agriculture and Agri-Food Canada, 960 Carling Avenue, Ottawa, ON K1A 0C6 Canada
                [ ]CNRS - UMR 5175 CEFE (CNRS, Université Montpellier 2), 1919 Route de Mende, 34293 Montpellier, France
                [ ]IRD, UMR 237 IMBE (IRD, Aix-Marseille Université, CNRS, Université d’Avignon et des pays de Vaucluse), Centre IRD de Nouméa, 98848 Nouméa, Nouvelle-Calédonie France
                [ ]Department of Biological and Environmental Sciences, University of Gothenburg, Box 461, SE-405 30 Göteborg, Sweden
                Article
                220
                10.1186/s12862-014-0220-1
                4210489
                25331733
                1756aaf4-65c1-4dbd-ab97-a9389dd610be
                © Kergoat et al.; licensee BioMed Central Ltd. 2014

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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.

                History
                : 8 August 2014
                : 6 October 2014
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2014

                Evolutionary Biology
                cretaceous-palaeogene mass extinction,cretaceous terrestrial revolution,dating analyses,diversification analyses,environmental changes,palaeoclimates,tenebrionidae

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