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      Quantifying the unquantifiable: why Hymenoptera, not Coleoptera, is the most speciose animal order

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          Abstract

          Background

          We challenge the oft-repeated claim that the beetles (Coleoptera) are the most species-rich order of animals. Instead, we assert that another order of insects, the Hymenoptera, is more speciose, due in large part to the massively diverse but relatively poorly known parasitoid wasps. The idea that the beetles have more species than other orders is primarily based on their respective collection histories and the relative availability of taxonomic resources, which both disfavor parasitoid wasps. Though it is unreasonable to directly compare numbers of described species in each order, the ecology of parasitic wasps—specifically, their intimate interactions with their hosts—allows for estimation of relative richness.

          Results

          We present a simple logical model that shows how the specialization of many parasitic wasps on their hosts suggests few scenarios in which there would be more beetle species than parasitic wasp species. We couple this model with an accounting of what we call the “genus-specific parasitoid–host ratio” from four well-studied genera of insect hosts, a metric by which to generate extremely conservative estimates of the average number of parasitic wasp species attacking a given beetle or other insect host species.

          Conclusions

          Synthesis of our model with data from real host systems suggests that the Hymenoptera may have 2.5–3.2× more species than the Coleoptera. While there are more described species of beetles than all other animals, the Hymenoptera are almost certainly the larger order.

          Electronic supplementary material

          The online version of this article (10.1186/s12898-018-0176-x) contains supplementary material, which is available to authorized users.

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          Most cited references92

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          How many species are there on Earth?

          R M May (1988)
          This article surveys current answers to the factual question posed in the title and reviews the kinds of information that are needed to make these answers more precise. Various factors affecting diversity are also reviewed. These include the structure of food webs, the relative abundance of species, the number of species and of individuals in different categories of body size, along with other determinants of the commonness and rarity of organisms.
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            Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections.

            We DNA barcoded 2,597 parasitoid wasps belonging to 6 microgastrine braconid genera reared from parapatric tropical dry forest, cloud forest, and rain forest in Area de Conservación Guanacaste (ACG) in northwestern Costa Rica and combined these data with records of caterpillar hosts and morphological analyses. We asked whether barcoding and morphology discover the same provisional species and whether the biological entities revealed by our analysis are congruent with wasp host specificity. Morphological analysis revealed 171 provisional species, but barcoding exposed an additional 142 provisional species; 95% of the total is likely to be undescribed. These 313 provisional species are extraordinarily host specific; more than 90% attack only 1 or 2 species of caterpillars out of more than 3,500 species sampled. The most extreme case of overlooked diversity is the morphospecies Apanteles leucostigmus. This minute black wasp with a distinctive white wing stigma was thought to parasitize 32 species of ACG hesperiid caterpillars, but barcoding revealed 36 provisional species, each attacking one or a very few closely related species of caterpillars. When host records and/or within-ACG distributions suggested that DNA barcoding had missed a species-pair, or when provisional species were separated only by slight differences in their barcodes, we examined nuclear sequences to test hypotheses of presumptive species boundaries and to further probe host specificity. Our iterative process of combining morphological analysis, ecology, and DNA barcoding and reiteratively using specimens maintained in permanent collections has resulted in a much more fine-scaled understanding of parasitoid diversity and host specificity than any one of these elements could have produced on its own.
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              Host races in plant-feeding insects and their importance in sympatric speciation.

              The existence of a continuous array of sympatric biotypes - from polymorphisms, through ecological or host races with increasing reproductive isolation, to good species - can provide strong evidence for a continuous route to sympatric speciation via natural selection. Host races in plant-feeding insects, in particular, have often been used as evidence for the probability of sympatric speciation. Here, we provide verifiable criteria to distinguish host races from other biotypes: in brief, host races are genetically differentiated, sympatric populations of parasites that use different hosts and between which there is appreciable gene flow. We recognize host races as kinds of species that regularly exchange genes with other species at a rate of more than ca. 1% per generation, rather than as fundamentally distinct taxa. Host races provide a convenient, although admittedly somewhat arbitrary intermediate stage along the speciation continuum. They are a heuristic device to aid in evaluating the probability of speciation by natural selection, particularly in sympatry. Speciation is thereby envisaged as having two phases: (i) the evolution of host races from within polymorphic, panmictic populations; and (ii) further reduction of gene flow between host races until the diverging populations can become generally accepted as species. We apply this criterion to 21 putative host race systems. Of these, only three are unambiguously classified as host races, but a further eight are strong candidates that merely lack accurate information on rates of hybridization or gene flow. Thus, over one-half of the cases that we review are probably or certainly host races, under our definition. Our review of the data favours the idea of sympatric speciation via host shift for three major reasons: (i) the evolution of assortative mating as a pleiotropic by-product of adaptation to a new host seems likely, even in cases where mating occurs away from the host; (ii) stable genetic differences in half of the cases attest to the power of natural selection to maintain multilocus polymorphisms with substantial linkage disequilibrium, in spite of probable gene flow; and (iii) this linkage disequilibrium should permit additional host adaptation, leading to further reproductive isolation via pleiotropy, and also provides conditions suitable for adaptive evolution of mate choice (reinforcement) to cause still further reductions in gene flow. Current data are too sparse to rule out a cryptic discontinuity in the apparently stable sympatric route from host-associated polymorphism to host-associated species, but such a hiatus seems unlikely on present evidence. Finally, we discuss applications of an understanding of host races in conservation and in managing adaptation by pests to control strategies, including those involving biological control or transgenic parasite-resistant plants.
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                Author and article information

                Contributors
                andrew-forbes@uiowa.edu
                Journal
                BMC Ecol
                BMC Ecol
                BMC Ecology
                BioMed Central (London )
                1472-6785
                12 July 2018
                12 July 2018
                2018
                : 18
                : 21
                Affiliations
                ISNI 0000 0004 1936 8294, GRID grid.214572.7, Department of Biology, , University of Iowa, ; 434 Biology Building, Iowa City, IA 52242 USA
                Article
                176
                10.1186/s12898-018-0176-x
                6042248
                30001194
                c9fa723a-3d74-41a7-be6e-5d165409bc14
                © 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.

                History
                : 24 March 2018
                : 13 June 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000155, Division of Environmental Biology;
                Award ID: 1145355
                Award ID: 1542269
                Award Recipient :
                Categories
                Correspondence
                Custom metadata
                © The Author(s) 2018

                Ecology
                beetles,inordinate fondness,animal diversity,parasitic wasps,parasitoids,species richness
                Ecology
                beetles, inordinate fondness, animal diversity, parasitic wasps, parasitoids, species richness

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