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      Maternal care in Acanthosomatinae (Insecta: Heteroptera: Acanthosomatidae)—correlated evolution with morphological change

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          Abstract

          Background

          Maternal care (egg-nymph guarding behavior) has been recorded in some genera of Acanthosomatidae. However, the origin of the maternal care in the family has remained unclear due to the lack of phylogenetic hypotheses. Another reproductive mode is found in non-caring species whose females smear their eggs before leaving them. They possess pairs of complex organs on the abdominal venter called Pendergrast’s organ (PO) and spread the secretion of this organ onto each egg with their hind legs, which is supposed to provide a protective function against enemies. Some authors claim that the absence of PO may be associated with the presence of maternal care. No study, however, has tested this hypothesis of a correlated evolution between the two traits.

          Results

          We reconstructed the molecular phylogeny of the subfamily Acanthosomatinae using five genetic markers sequenced from 44 species and one subspecies with and without maternal care. Eight additional species from the other two acanthosomatid subfamilies were included as outgroups. Our results indicated that maternal care has evolved independently at least three times within Acanthosomatinae and once in the outgroup species. Statistical tests for correlated evolution showed that the presence of maternal care is significantly correlated with the secondary loss or reduction of PO. Ancestral state reconstruction for the node of Acanthosoma denticaudum (a non-caring species in which egg smearing with developed POs occurs) and A. firmatum (a caring species with reduced POs) suggested egg smearing was still present in their most recent common ancestor and that maternal care in A. firmatum has evolved relatively recently.

          Conclusions

          We showed that maternal care is an apomorphic trait that has arisen multiple times from the presence of PO within the subfamily Acanthosomatinae. The acquisition of maternal care is correlated with the reduction or loss of PO, which suggests an evolutionary trade-off between the two traits resulting from physiological costs. This prediction also implies that presence of maternal care can be highly expected for those groups lacking behavioral data, which invariably also lack the organ. No secondary loss of maternal care was detected in the present tree. We suggest that the loss of maternal care may be suppressed due to the vulnerability of the PO-free condition, which thus maintains maternal care.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12862-015-0537-4) contains supplementary material, which is available to authorized users.

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          Most cited references130

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                Author and article information

                Contributors
                jingfu.tsai@gmail.com
                skudo@naruto-u.ac.jp
                psocid@res.agr.hokudai.ac.jp
                Journal
                BMC Evol Biol
                BMC Evol. Biol
                BMC Evolutionary Biology
                BioMed Central (London )
                1471-2148
                19 November 2015
                19 November 2015
                2015
                : 15
                Affiliations
                [ ]Systematic Entomology, School of Agriculture, Hokkaido University, Sapporo, 060-8589 Japan
                [ ]Department of Biology, Naruto University of Education, Naruto, Tokushima 772-8502 Japan
                [ ]Department of Biology, National Museum of Natural Science, Taichung, 40427 Taiwan
                Article
                537
                10.1186/s12862-015-0537-4
                4653913
                e47b244e-bf81-4088-914f-2c4d4046f586
                © Tsai et al. 2015

                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) 2015

                Evolutionary Biology
                molecular phylogeny,acanthosomatinae,maternal care,egg guarding,egg smearing,pendergrast’s organ,correlated evolution

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