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

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.

The genetic basis of a novel reproductive strategy in Sulawesi ricefishes: How modularity and a low number of loci shape pelvic brooding

“…This means, the more O. nigrimas-like the body shape was, the shorter was the pelvic fin. This result was not surprising, since the pelvic fins of females O. nigrimas are significantly shorter in relation to standard length as the pelvic fins of females O. eversi (Spanke et al 2021). The pelvic fin length and the body shape followed a O. nigrimas-O.…”

“…All areas were also measured in ImageJ, version 1.51u. Rib 12 length (R12) was chosen to be measured, because it is shortened in females of pelvic brooding species (Spanke et al 2021). The landmarks on rib 12 were used to measure its length from vertebra to tip (Fig.…”

Genetic basis for the evolution of pelvic‐fin brooding, a new mode of reproduction, in a Sulawesian fish

“…For example, longer pelvic fins might not be disadvantageous to females (Spanke et al, 2021). In contrast, it is considered that a deeper abdominal concavity could reduce egg clutch size (Spanke et al, 2021). The presence or absence of fitness valleys should be rigorously tested by experimental manipulations of each characteristic, such as, for example, by cutting female pelvic fins or altering the maturation cycles of oocytes with hormonal treatment.…”

“…One possibility is that the multiple traits necessary for this mode of reproduction evolved one by one, rather than at the same time, gradually and possibly without passing through fitness valleys during early combinations of these functional traits. For example, longer pelvic fins might not be disadvantageous to females (Spanke et al, 2021). In contrast, it is considered that a deeper abdominal concavity could reduce egg clutch size (Spanke et al, 2021).…”

Contribution of hybridization to the evolution of a derived reproductive strategy in ricefishes

“…Females of pelvic-brooding ricefish species carry a cluster of eggs attached to their gonoduct for up to three weeks, until the fry hatches (Kottelat 1990). They have elongated pelvic fins and shorter ribs, forming a concavity where the egg cluster is situated (Spanke et al 2021;Kottelat 1990).…”