Parental care drives the evolution of male reproductive accessory glands across ray-finned fishes.

Abstract

Reproductive accessory glands are organs involved in reproduction that do not directly produce or release gametes but can play crucial roles in securing reproductive success. In fishes, the two leading hypotheses about why accessory glands evolved are 1) in response to sperm competition, or 2) to facilitate parental care activities. Here, we investigate the evolutionary history of accessory glands and test these hypotheses by estimating quantitative differences in evolutionary rates. We found that accessory glands are present in 116 of the 607 sampled species of ray-finned fishes, representing 26/267 families. We estimated that accessory glands have arisen independently ~20 times and that these glands were gained 5.8 times faster in lineages with male parental care, compared to those without male care, supporting the hypothesis that they evolved to facilitate care. In contrast, group spawning, used as a proxy for sperm competition risk, seemed to select against the evolution of accessory glands, as lineages exhibiting group spawning gained accessory glands 3.9 times slower than those with pair spawning (though this failed to reach statistical significance). This study provides new insights into the evolutionary history of accessory glands in fishes and highlights the importance of parental care in shaping reproductive anatomy.