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      Timing and Patterns in the Taxonomic Diversification of Lepidoptera (Butterflies and Moths)

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          Abstract

          The macroevolutionary history of the megadiverse insect order Lepidoptera remains little-known, yet coevolutionary dynamics with their angiospermous host plants are thought to have influenced their diversification significantly. We estimate the divergence times of all higher-level lineages of Lepidoptera, including most extant families. We find that the diversification of major lineages in Lepidoptera are approximately equal in age to the crown group of angiosperms and that there appear to have been three significant increases in diversification rates among Lepidoptera over evolutionary time: 1) at the origin of the crown group of Ditrysia about 150 million years ago (mya), 2) at the origin of the stem group of Apoditrysia about 120 mya and finally 3) a spectacular increase at the origin of the stem group of the quadrifid noctuoids about 70 mya. In addition, there appears to be a significant increase in diversification rate in multiple lineages around 90 mya, which is concordant with the radiation of angiosperms. Almost all extant families appear to have begun diversifying soon after the Cretaceous/Paleogene event 65.51 mya.

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          A Total-Evidence Approach to Dating with Fossils, Applied to the Early Radiation of the Hymenoptera

          Phylogenies are usually dated by calibrating interior nodes against the fossil record. This relies on indirect methods that, in the worst case, misrepresent the fossil information. Here, we contrast such node dating with an approach that includes fossils along with the extant taxa in a Bayesian total-evidence analysis. As a test case, we focus on the early radiation of the Hymenoptera, mostly documented by poorly preserved impression fossils that are difficult to place phylogenetically. Specifically, we compare node dating using nine calibration points derived from the fossil record with total-evidence dating based on 343 morphological characters scored for 45 fossil (4--20 complete) and 68 extant taxa. In both cases we use molecular data from seven markers (∼5 kb) for the extant taxa. Because it is difficult to model speciation, extinction, sampling, and fossil preservation realistically, we develop a simple uniform prior for clock trees with fossils, and we use relaxed clock models to accommodate rate variation across the tree. Despite considerable uncertainty in the placement of most fossils, we find that they contribute significantly to the estimation of divergence times in the total-evidence analysis. In particular, the posterior distributions on divergence times are less sensitive to prior assumptions and tend to be more precise than in node dating. The total-evidence analysis also shows that four of the seven Hymenoptera calibration points used in node dating are likely to be based on erroneous or doubtful assumptions about the fossil placement. With respect to the early radiation of Hymenoptera, our results suggest that the crown group dates back to the Carboniferous, ∼309 Ma (95% interval: 291--347 Ma), and diversified into major extant lineages much earlier than previously thought, well before the Triassic. [Bayesian inference; fossil dating; morphological evolution; relaxed clock; statistical phylogenetics.]
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            Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates.

            The uneven distribution of species richness is a fundamental and unexplained pattern of vertebrate biodiversity. Although species richness in groups like mammals, birds, or teleost fishes is often attributed to accelerated cladogenesis, we lack a quantitative conceptual framework for identifying and comparing the exceptional changes of tempo in vertebrate evolutionary history. We develop MEDUSA, a stepwise approach based upon the Akaike information criterion for detecting multiple shifts in birth and death rates on an incompletely resolved phylogeny. We apply MEDUSA incompletely to a diversity tree summarizing both evolutionary relationships and species richness of 44 major clades of jawed vertebrates. We identify 9 major changes in the tempo of gnathostome diversification; the most significant of these lies at the base of a clade that includes most of the coral-reef associated fishes as well as cichlids and perches. Rate increases also underlie several well recognized tetrapod radiations, including most modern birds, lizards and snakes, ostariophysan fishes, and most eutherian mammals. In addition, we find that large sections of the vertebrate tree exhibit nearly equal rates of origination and extinction, providing some of the first evidence from molecular data for the importance of faunal turnover in shaping biodiversity. Together, these results reveal living vertebrate biodiversity to be the product of volatile turnover punctuated by 6 accelerations responsible for >85% of all species as well as 3 slowdowns that have produced "living fossils." In addition, by revealing the timing of the exceptional pulses of vertebrate diversification as well as the clades that experience them, our diversity tree provides a framework for evaluating particular causal hypotheses of vertebrate radiations.
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              Accounting for calibration uncertainty in phylogenetic estimation of evolutionary divergence times.

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                25 November 2013
                : 8
                : 11
                : e80875
                Affiliations
                [1 ]Department of Biology, University of Turku, Turku, Finland
                [2 ]Department of Zoology, Stockholm University, Stockholm, Sweden
                BiK-F Biodiversity and Climate Research Center, Germany
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: NW. Performed the experiments: NW CP CWW. Analyzed the data: NW CP CWW. Wrote the paper: NW CP CWW.

                Article
                PONE-D-13-33887
                10.1371/journal.pone.0080875
                3839996
                24282557
                1909fff0-1888-44e9-8eb2-c58635c511b2
                Copyright @ 2013

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 6 August 2013
                : 7 October 2013
                Page count
                Pages: 8
                Funding
                This study has been funded by Kone Foundation (NW and CP) and the Academy of Finland (CWW). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article

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