Abstract

BackgroundPelvic 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.ResultsThe 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.ConclusionsWe 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.

Highlights

  • Pelvic brooding is a form of uni-parental care, and likely evolved in parallel in two lineages of Sulawesi ricefishes

  • Specific ribs are shorter in females of pelvic brooding ricefishes Intersexual differences in rib length were present in pelvic brooding ricefish species (O. eversi, O. sarasinorum and A. oophorus) and interspecific differences were present between females of pelvic brooding and transfer brooding (O. celebensis, O. nigrimas, O. wolasi, O. matanensis) ricefishes (Figs. 2, 3)

  • A significant negative correlation of rib length and the interaction of sex and reproductive strategy was found for rib rib 0 (R0), located at the pelvic girdle (Fig. 5a), with males of pelvic brooding species having shorter ribs than conspecific females (LMM: p = 0.0128, ­F1,19.8 = 7.4883, β = − 0.74)

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Summary

Introduction

Pelvic brooding is a form of uni-parental care, and likely evolved in parallel in two lineages of Sulawesi ricefishes. 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. External bearing [16, 17] or egg brooding [18] is a form of parental care in which eggs are carried externally, attached to the parents body, sometimes by specialized structures, or in the parents mouth In some of these cases, eggs are nurtured [19] by either of the parents. Carrying the brood may require anatomical adaptations, which can include the evolution of highly specialized tissues and organs, like brood pouches and incubating areas in seahorses and pipefishes [20, 21]

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