Complex sexually dimorphic traits shape the parallel evolution of a novel reproductive strategy in Sulawesi ricefishes (Adrianichthyidae).

Tobias Spanke, Leon Hilgers, Benjamin Wipfler, Jana M Flury, Arne W Nolte, Ilham V Utama, Bernhard Misof, Fabian Herder, Julia Schwarzer
Author Information
  1. Tobias Spanke: Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113, Bonn, Germany.
  2. Leon Hilgers: Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113, Bonn, Germany.
  3. Benjamin Wipfler: Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113, Bonn, Germany.
  4. Jana M Flury: Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113, Bonn, Germany.
  5. Arne W Nolte: Carl Von Ossietzky Universität Oldenburg, AG Ökologische Genomik, Carl von Ossietzky-Str. 9-11, 26111, Oldenburg, Germany.
  6. Ilham V Utama: Ichthyology Laboratory, Indonesian Institute of Sciences (LIPI), JL. Raya Jakarta-Bogor Km. 46, Cibinong, 16911, Indonesia.
  7. Bernhard Misof: Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113, Bonn, Germany.
  8. Fabian Herder: Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113, Bonn, Germany.
  9. Julia Schwarzer: Zoologisches Forschungsmuseum Alexander Koenig, Adenauerallee 160, 53113, Bonn, Germany. j.schwarzer@leibniz-zfmk.de. ORCID

Abstract

BACKGROUND: Pelvic brooding is a form of uni-parental care, and likely evolved in parallel in two lineages of Sulawesi ricefishes. Contrary to all other ricefishes, females of pelvic brooding species do not deposit eggs at a substrate (transfer brooding), but carry them until the fry hatches. We assume that modifications reducing the costs of egg carrying are beneficial for pelvic brooding females, but likely disadvantageous in conspecific males, which might be resolved by the evolution of sexual dimorphism via sexual antagonistic selection. Thus we hypothesize that the evolution of pelvic brooding gave rise to female-specific skeletal adaptations that are shared by both pelvic brooding lineages, but are absent in conspecific males and transfer brooding species. To tackle this, we combine 3D-imaging and morphometrics to analyze skeletal adaptations to pelvic brooding.
RESULTS: The morphology of skeletal traits correlated with sex and brooding strategy across seven ricefish species. Pelvic brooding females have short ribs caudal of the pelvic girdle forming a ventral concavity and clearly elongated and thickened pelvic fins compared to both sexes of transfer brooding species. The ventral concavity limits the body cavity volume in female pelvic brooders. Thus body volumes are smaller compared to males in pelvic brooding species, a pattern sharply contrasted by transfer brooding species.
CONCLUSIONS: We showed in a comparative framework that highly similar, sexually dimorphic traits evolved in parallel in both lineages of pelvic brooding ricefish species. Key traits, present in all pelvic brooding females, were absent or much less pronounced in conspecific males and both sexes of transfer brooding species, indicating that they are non-beneficial or even maladaptive for ricefishes not providing extended care. We assume that the combination of ventral concavity and robust, elongated fins reduces drag of brooding females and provides protection and stability to the egg cluster. Thus ricefishes are one of the rare examples where environmental factors rather than sexual selection shaped the evolution of sexually dimorphic skeletal adaptations.

Keywords

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MeSH Term

Animals
Female
Indonesia
Male
Oryzias
Phenotype
Reproduction
Sex Characteristics

Word Cloud

Created with Highcharts 10.0.0broodingpelvicspeciesricefishesfemalestransfermalesevolutionskeletaltraitscareparallellineagesconspecificsexualselectionThusadaptationsventralconcavitysexuallydimorphicPelviclikelyevolvedSulawesiassumeeggdimorphismantagonisticabsentstrategyricefishelongatedfinscomparedsexesbodySexualBACKGROUND:formuni-parentaltwoContrarydepositeggssubstratecarryfryhatchesmodificationsreducingcostscarryingbeneficialdisadvantageousmightresolvedviahypothesizegaverisefemale-specificsharedtacklecombine3D-imagingmorphometricsanalyzeRESULTS:morphologycorrelatedsexacrosssevenshortribscaudalgirdleformingclearlythickenedlimitscavityvolumefemalebroodersvolumessmallerpatternsharplycontrastedCONCLUSIONS:showedcomparativeframeworkhighlysimilarKeypresentmuchlesspronouncedindicatingnon-beneficialevenmaladaptiveprovidingextendedcombinationrobustreducesdragprovidesprotectionstabilityclusteronerareexamplesenvironmentalfactorsrathershapedComplexshapenovelreproductiveAdrianichthyidaeAdrianichthysMaternalOryziasRiblengthRibs

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