{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,16]],"date-time":"2025-10-16T07:04:39Z","timestamp":1760598279194,"version":"3.37.3"},"reference-count":63,"publisher":"Oxford University Press (OUP)","issue":"6","license":[{"start":{"date-parts":[[2024,3,12]],"date-time":"2024-03-12T00:00:00Z","timestamp":1710201600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","award":["754290"],"award-info":[{"award-number":["754290"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"German Research Foundation","doi-asserted-by":"publisher","award":["BL 1355\/4-1"],"award-info":[{"award-number":["BL 1355\/4-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,5,29]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Bilateral symmetry is widespread across animals, yet, among bilaterians, many cases of conspicuous asymmetries evolved. This means that bilaterally homologous structures on the left and right sides display divergent phenotypes. The evolution of such divergent phenotypes between otherwise similarly shaped structures can be thought to be favored by modularity, but this has rarely been studied in the context of left-right differences. Here, we provide an empirical example, using geometric morphometrics to assess patterns of asymmetry and covariation between landmark partitions in a grasshopper with conspicuously asymmetric mandibles. Our morphometric data confirm the presence of strictly directional conspicuous asymmetry in the mandibles and surrounding structures. Covariance patterns and tests hint at a strong integration between mandibles despite their divergent morphologies, and variational modularity with the head capsule. While mandibles have been selected to achieve a key-and-lock morphology by having interlocking shapes, the developmental modularity required to achieve this seems to be overwritten by developmental and\/or functional integration, allowing the precise matching required for feeding. The consequent conflicting covariation patterns are reminiscent of the palimpsest model. Finally, the degree of directional asymmetry appears to be under selection, although we find no relationship between bite force and mandible shape or asymmetry.<\/jats:p>","DOI":"10.1093\/evolut\/qpae040","type":"journal-article","created":{"date-parts":[[2024,3,12]],"date-time":"2024-03-12T09:49:21Z","timestamp":1710236961000},"page":"1078-1091","source":"Crossref","is-referenced-by-count":5,"title":["Linking shape conspicuous asymmetry with shape covariation patterns and performance in the insect head and mandibles"],"prefix":"10.1093","volume":"78","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0060-9660","authenticated-orcid":false,"given":"Samuel","family":"Ginot","sequence":"first","affiliation":[{"name":"Bonner Institut f\u00fcr Organismische Biologie, Universit\u00e4t Bonn , Bonn , Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Simon","family":"Sommerfeld","sequence":"additional","affiliation":[{"name":"Bonner Institut f\u00fcr Organismische Biologie, Universit\u00e4t Bonn , Bonn , Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alexander","family":"Blanke","sequence":"additional","affiliation":[{"name":"Bonner Institut f\u00fcr Organismische Biologie, Universit\u00e4t Bonn , Bonn , Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2024,3,12]]},"reference":[{"key":"2024052916223392000_CIT0001","first-page":"565","article-title":"Evaluating modularity in morphometric data: Challenges with the RV coefficient and a new test measure","volume-title":"Methods in Ecology and Evolution","author":"Adams","year":"2016"},{"volume-title":"geomorph: Software for geometric morphometric analyses (4.0.4) [R]","year":"2022","author":"Adams","key":"2024052916223392000_CIT0002"},{"key":"2024052916223392000_CIT0003","first-page":"135","article-title":"Asymmetry in the fossil record","volume-title":"European Review","author":"Babcock","year":"2005"},{"key":"2024052916223392000_CIT0004","first-page":"2355","article-title":"geomorph v4.0 and gmShiny: Enhanced analytics and a new graphical interface for a comprehensive morphometric experience","volume-title":"Methods in Ecology and Evolution","author":"Baken","year":"2021"},{"issue":"2","key":"2024052916223392000_CIT0005","first-page":"325","article-title":"The tribe Licinini (Coleoptera: Carabidae): A review of the genus-groups and of the species of selected genera","volume":"100","author":"Ball","year":"1992","journal-title":"Journal of the New York Entomological Society"},{"key":"2024052916223392000_CIT0006","first-page":"1789","article-title":"Breaking symmetry: Fluctuating asymmetry and geometric Morphometrics as tools for evaluating developmental instability under diverse agroecosystems","volume-title":"Symmetry","author":"Ben\u00edtez","year":"2020"},{"key":"2024052916223392000_CIT0007","first-page":"1","article-title":"The development of handedness in left\/right asymmetry","volume-title":"Development","author":"Brown","year":"1990"},{"key":"2024052916223392000_CIT0008","first-page":"107","article-title":"The structure and wear of the mandibles in some African grasshoppers","volume-title":"Proceedings of the Zoological Society of London","author":"Chapman","year":"1964"},{"key":"2024052916223392000_CIT0009","first-page":"225","article-title":"Asymmetry drives modularity of the skull in the common dolphin (Delphinus delphis)","volume-title":"Biological Journal of the Linnean Society","author":"Churchill","year":"2019"},{"volume-title":"Morphometrics with R","year":"2008","author":"Claude","key":"2024052916223392000_CIT0010"},{"key":"2024052916223392000_CIT0011","first-page":"317","article-title":"The biomechanics of chewing and plant fracture: Mechanisms and implications","volume-title":"Advances in insect physiology","author":"Clissold","year":"2007"},{"key":"2024052916223392000_CIT0012","first-page":"20122863","article-title":"The evolutionary origins of modularity","volume-title":"Proceedings of the Royal Society of London, Series B: Biological Sciences","author":"Clune","year":"2013"},{"key":"2024052916223392000_CIT0013","first-page":"1772","article-title":"RRPP: An R package for fitting linear models to high-dimensional data using residual randomization","volume-title":"Methods in Ecology and Evolution","author":"Collyer","year":"2018"},{"year":"2021","author":"Collyer","key":"2024052916223392000_CIT0014"},{"key":"2024052916223392000_CIT0015","first-page":"1345","article-title":"Cranial development and directional asymmetry in Commerson\u2019s dolphin, Cephalorhynchus commersonii commersonii: 3D geometric morphometric approach","volume-title":"Journal of Mammalogy","author":"del Castillo","year":"2016"},{"key":"2024052916223392000_CIT0016","first-page":"203","article-title":"Skull ontogeny and modularity in two species of Lagenorhynchus: Morphological and ecological implications","volume-title":"Journal of Morphology","author":"del Castillo","year":"2017"},{"key":"2024052916223392000_CIT0017","first-page":"22","article-title":"Untangling the relationship between developmental and evolutionary integration","volume-title":"Seminars in Cell & Developmental Biology","author":"Evans","year":"2023"},{"key":"2024052916223392000_CIT0018","first-page":"e2101330118","article-title":"Integration drives rapid phenotypic evolution in flatfishes","volume-title":"Proceedings of the National Academy of Sciences of the United States of America","author":"Evans","year":"2021"},{"key":"2024052916223392000_CIT0019","first-page":"2580","article-title":"A fly in a tube: Macroevolutionary expectations for integrated phenotypes","volume-title":"Evolution","author":"Felice","year":"2018"},{"key":"2024052916223392000_CIT0020","doi-asserted-by":"crossref","DOI":"10.1242\/jeb.246341","article-title":"A comparison of dissection and 3D approaches to estimate muscle physiological cross-sectional area, validated by in vivo bite forces","volume-title":"Journal of Experimental Biology","author":"Ginot","year":"2023"},{"issue":"5","key":"2024052916223392000_CIT0021","first-page":"468","article-title":"Asymmetry in lobster claws","volume":"77","author":"Govind","year":"1989","journal-title":"American Naturalist"},{"key":"2024052916223392000_CIT0022","first-page":"321","article-title":"Form and function of the asymmetric chelae in blue crabs with normal and reversed handedness","volume-title":"The Biological Bulletin","author":"Govind","year":"1985"},{"key":"2024052916223392000_CIT0023","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1007\/978-94-011-0830-0_10","article-title":"Antisymmetry, directional asymmetry, and dynamic morphogenesis","volume-title":"Developmental instability: Its origins and evolutionary implications","author":"Graham","year":"1994"},{"key":"2024052916223392000_CIT0024","first-page":"355","article-title":"Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation","volume-title":"Evolutionary Biology","author":"Hallgr\u00edmsson","year":"2009"},{"issue":"2\u20133","key":"2024052916223392000_CIT0025","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1016\/S0303-2647(02)00132-6","article-title":"Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability","volume":"69","author":"Hansen","year":"2003","journal-title":"Biosystems"},{"key":"2024052916223392000_CIT0026","first-page":"168","article-title":"On adaptive accuracy and precision in natural populations","volume-title":"The American Naturalist","author":"Hansen","year":"2006"},{"key":"2024052916223392000_CIT0027","first-page":"15","article-title":"Asymmetry of the nasofacial skull in toothed whales (Odontoceti)","volume-title":"Journal of Zoology","author":"Huggenberger","year":"2017"},{"key":"2024052916223392000_CIT0028","first-page":"285","article-title":"Shape asymmetry\u2014What\u2019s new","volume-title":"Emerging Topics in Life Sciences","author":"Klingenberg","year":"2022"},{"key":"2024052916223392000_CIT0029","first-page":"11","article-title":"Inferring developmental modularity from morphological integration: Analysis of individual variation and asymmetry in bumblebee wings","volume-title":"The American Naturalist","author":"Klingenberg","year":"2001"},{"key":"2024052916223392000_CIT0030","first-page":"1255","article-title":"Left-right asymmetry of fly wings and the evolution of body axes","volume-title":"Proceedings of the Royal Society of London, Series B: Biological Sciences","author":"Klingenberg","year":"1998"},{"key":"2024052916223392000_CIT0031","first-page":"126108","article-title":"Cranial asymmetry in odontocetes: A facilitator of sonic exploration","volume-title":"Zoology (Jena, Germany)","author":"Laeta","year":"2023"},{"key":"2024052916223392000_CIT0032","first-page":"20221090","article-title":"The ontogeny of asymmetry in echolocating whales","volume-title":"Proceedings of the Royal Society of London, Series B: Biological Sciences","author":"Lanzetti","year":"2022"},{"volume-title":"MorphoDig, An open-source 3D freeware dedicated to biology","year":"2018","author":"Lebrun","key":"2024052916223392000_CIT0033"},{"key":"2024052916223392000_CIT0034","first-page":"370","article-title":"Bilateral linkage of monomorphic and dimorphic limb sizes in fiddler crabs","volume-title":"Biological Journal of the Linnean Society","author":"Levinton","year":"2016"},{"volume-title":"paleomorph: Geometric morphometric tools for paleobiology (0.1.4) [R]","year":"2017","author":"Lucas","key":"2024052916223392000_CIT0035"},{"key":"2024052916223392000_CIT0036","first-page":"539","article-title":"Breaking symmetry: The marine environment, prey size, and the evolution of asymmetry in cetacean skulls","volume-title":"Anatomical Record (Hoboken, N. J.: 2007)","author":"Macleod","year":"2007"},{"issue":"1","key":"2024052916223392000_CIT0037","first-page":"177","article-title":"Organizer and axes formation as a self-organizing process","volume":"45","author":"Meinhardt","year":"2001","journal-title":"The International Journal of Developmental Biology"},{"key":"2024052916223392000_CIT0038","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-642-36160-9","volume-title":"Arthropod biology and evolution: Molecules, development, morphology","author":"Minelli","year":"2013"},{"key":"2024052916223392000_CIT0039","first-page":"1185","article-title":"Fluctuating asymmetry in male sexual ornaments may reliably reveal male quality","volume-title":"Animal Behaviour","author":"M\u00f8ller","year":"1990"},{"key":"2024052916223392000_CIT0040","first-page":"eaax9935","article-title":"Evolution of brain lateralization: A shared hominid pattern of endocranial asymmetry is much more variable in humans than in great apes","volume-title":"Science Advances","author":"Neubauer","year":"2020"},{"key":"2024052916223392000_CIT0041","first-page":"173","article-title":"Fighting does not influence the morphological integration of crustacean claws (Decapoda: Aeglidae)","volume-title":"Biological Journal of the Linnean Society","author":"Nogueira","year":"2022"},{"key":"2024052916223392000_CIT0042","doi-asserted-by":"crossref","first-page":"335","DOI":"10.1007\/978-94-011-0830-0_26","article-title":"Fluctuating asymmetry analyses: A primer","volume-title":"Developmental instability: Its origins and evolutionary implications","author":"Palmer","year":"1994"},{"key":"2024052916223392000_CIT0043","first-page":"14279","article-title":"From symmetry to asymmetry: Phylogenetic patterns of asymmetry variation in animals and their evolutionary significance","volume-title":"Proceedings of the National Academy of Sciences of the United States of America","author":"Palmer","year":"1996"},{"key":"2024052916223392000_CIT0044","first-page":"828","article-title":"Symmetry breaking and the evolution of development","volume-title":"Science","author":"Palmer","year":"2004"},{"key":"2024052916223392000_CIT0045","first-page":"20150417","article-title":"What determines direction of asymmetry: Genes, environment or chance","volume-title":"Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences","author":"Palmer","year":"2016"},{"key":"2024052916223392000_CIT0046","first-page":"20150984","article-title":"Bridging the gap: Wound healing in insects restores mechanical strength by targeted cuticle deposition","volume-title":"Journal of the Royal Society Interface","author":"Parle","year":"2016"},{"key":"2024052916223392000_CIT0047","first-page":"247","article-title":"The effect of aging on the mechanical behaviour of cuticle in the locust Schistocerca gregaria","volume-title":"Journal of the Mechanical Behavior of Biomedical Materials","author":"Parle","year":"2017"},{"key":"2024052916223392000_CIT0048","first-page":"171","article-title":"Cranial shape and the modularity of hybridization in dingoes and dogs; hybridization does not spell the end for native morphology","volume-title":"Evolutionary Biology","author":"Parr","year":"2016"},{"key":"2024052916223392000_CIT0049","first-page":"2855","article-title":"On the adaptive accuracy of directional asymmetry in insect wing size","volume-title":"Evolution","author":"P\u00e9labon","year":"2008"},{"key":"2024052916223392000_CIT0050","first-page":"1740","article-title":"Directional and fluctuating asymmetry in the black-winged damselfly Calopteryx maculata (Beauvois) (Odonata: Calopterygidae)","volume-title":"Canadian Journal of Zoology","author":"Pither","year":"2000"},{"key":"2024052916223392000_CIT0051","first-page":"107","article-title":"Formation of the insect head involves lateral contribution of the intercalary segment, which depends on Tc-labial function","volume-title":"Developmental Biology","author":"Posnien","year":"2010"},{"key":"2024052916223392000_CIT0052","first-page":"89","article-title":"Antisymmetry in male fiddler crabs and the decision to feed or breed","volume-title":"Functional Ecology","author":"Pratt","year":"2002"},{"key":"2024052916223392000_CIT0053","first-page":"221066","article-title":"A biomechanical model for the relation between bite force and mandibular opening angle in arthropods","volume-title":"Royal Society Open Science","author":"P\u00fcffel","year":"2023"},{"key":"2024052916223392000_CIT0054","first-page":"20210424","article-title":"Morphological determinants of bite force capacity in insects: A biomechanical analysis of polymorphous leaf-cutter ants","volume-title":"Journal of the Royal Society Interface","author":"P\u00fcffel","year":"2021"},{"volume-title":"R: A language and environment for statistical computing (4.2.1)","year":"2022","author":"R Core Team","key":"2024052916223392000_CIT0055"},{"key":"2024052916223392000_CIT0056","first-page":"1938","article-title":"ForceX and ForceR: A mobile setup and R package to measure and analyse a wide range of animal closing forces","volume-title":"Methods in Ecology and Evolution","author":"R\u00fchr","year":"2022"},{"key":"2024052916223392000_CIT0057","first-page":"187","article-title":"Modularity and developmental stability in segmented animals: Variation in translational asymmetry in geophilomorph centipedes","volume-title":"Development Genes and Evolution","author":"Savriama","year":"2016"},{"key":"2024052916223392000_CIT0058","first-page":"17481","article-title":"The homogenous alternative to biomineralization: Zn- and Mn-rich materials enable sharp organismal \u201ctools\u201d that reduce force requirements","volume-title":"Scientific Reports","author":"Schofield","year":"2021"},{"key":"2024052916223392000_CIT0059","first-page":"22","article-title":"Chewing side preference\u2014Impact on facial symmetry, dentition and temporomandibular joint and its correlation with handedness","volume-title":"Journal of Orofacial Sciences","author":"Tiwari","year":"2017"},{"issue":"2","key":"2024052916223392000_CIT0060","doi-asserted-by":"crossref","first-page":"125","DOI":"10.2307\/2406192","article-title":"A study of fluctuating asymmetry","volume":"16","author":"Van Valen","year":"1962","journal-title":"Evolution"},{"key":"2024052916223392000_CIT0061","first-page":"967","article-title":"Perspective: Complex adaptations and the evolution of evolvability","volume-title":"Evolution","author":"Wagner","year":"1996"},{"key":"2024052916223392000_CIT0062","first-page":"921","article-title":"The road to modularity","volume-title":"Nature Reviews Genetics","author":"Wagner","year":"2007"},{"key":"2024052916223392000_CIT0063","first-page":"377","article-title":"What does modularity mean","volume-title":"Evolution & Development","author":"Zelditch","year":"2021"}],"container-title":["Evolution"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/evolut\/advance-article-pdf\/doi\/10.1093\/evolut\/qpae040\/57089048\/qpae040.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/evolut\/article-pdf\/78\/6\/1078\/57985815\/qpae040.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/evolut\/article-pdf\/78\/6\/1078\/57985815\/qpae040.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,29]],"date-time":"2024-05-29T16:23:55Z","timestamp":1716999835000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/evolut\/article\/78\/6\/1078\/7626311"}},"subtitle":[],"editor":[{"given":"Miriam","family":"Zelditch","sequence":"additional","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]},{"given":"Jason","family":"Wolf","sequence":"additional","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2024,3,12]]},"references-count":63,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2024,3,12]]},"published-print":{"date-parts":[[2024,5,29]]}},"URL":"https:\/\/doi.org\/10.1093\/evolut\/qpae040","relation":{},"ISSN":["0014-3820","1558-5646"],"issn-type":[{"type":"print","value":"0014-3820"},{"type":"electronic","value":"1558-5646"}],"subject":[],"published-other":{"date-parts":[[2024,6,1]]},"published":{"date-parts":[[2024,3,12]]}}}