Rapid Gamete Maturation and Social Modulation Shape Reproductive Dynamics in a Brood Parasitic Catfish.

Abstract

Obligatory brood parasitism requires specific reproductive adaptations in brood parasites to successfully exploit host reproduction. A key challenge is to precisely synchronize parasite egg laying with egg laying of the host. The Lake Tanganyika cuckoo catfish (<i>Synodontis multipunctatus</i>) exploits the mouthbrooding behavior of cichlids by rapidly intruding during host spawning and adding its own eggs to host clutches. Because host reproduction is highly unpredictable, cuckoo catfish must respond quickly when host spawning occurs. Such a reproductive strategy suggests the presence of adaptations in their reproductive biology that allow them to be able to participate in upcoming host spawning opportunities. Using a series of linked laboratory experiments, we investigated the reproductive physiology and social modulation of gamete maturation in cuckoo catfish, as well as reproductive skew during parasitic spawning events. We found that males consistently produced sperm with little inter-individual variation, indicating almost continuous readiness to reproduce. In contrast, females exhibited substantial variation in ovulation frequency and ovulated, on average, once a week. Social interactions significantly increased gamete maturation rates in both sexes, highlighting the role of group dynamics in facilitating reproductive readiness. Despite high gamete maturation rates in socially housed females, parasitism success during host spawning events was not predicted by prior gamete production frequency. Smaller and slimmer males achieved higher reproductive success, suggesting a possibility that agility and reduced anticipation of potential threat by the hosts may confer advantages under competitive conditions. Reproductive skew was low across the experiment, and most individuals participated in reproduction over the duration of the experiment. However, single spawning events were typically monopolized by a single pair. These findings demonstrate that cuckoo catfish reproduction is shaped by a combination of frequent gamete maturation, social facilitation of their reproductive physiology, and scramble competition over mating opportunities.