Parasitic cuckoo catfish exploit parental responses to stray offspring

Abstract

Interspecific brood parasitism occurs in several independent lineages of birds and social insects, putatively evolving from intraspecific brood parasitism. The cuckoo catfish, Synodontis multipunctatus , the only known obligatory non-avian brood parasite, exploits mouthbrooding cichlid fishes in Lake Tanganyika, despite the absence of parental care in its evolutionary lineage (family Mochokidae). Cuckoo catfish participate in host spawning events, with their eggs subsequently collected and brooded by parental cichlids, though they can later be selectively rejected by the host. One scenario for the origin of brood parasitism in cuckoo catfish is through predation of cichlid eggs during spawning, eventually resulting in a spatial and temporal match in oviposition by host and parasite. Here we demonstrate experimentally that, uniquely among all known brood parasites, cuckoo catfish have the capacity to re-infect their hosts at a late developmental stage following egg rejection. We show that cuckoo catfish offspring can survive outside the host buccal cavity and re-infect parental hosts at a later incubation phase by exploiting the strong parental instinct of hosts to collect stray offspring. This finding implies an alternative evolutionary origin for cuckoo catfish brood parasitism, with the parental response of host cichlids facilitating its evolution. This article is part of the theme issue ‘The coevolutionary biology of brood parasitism: from mechanism to pattern’.

The coevolutionary biology of brood parasitism: a call for integration

“…Polacik et al [17] Litman [23] Yang et al [57] Spottiswoode & Busch [58] Kaur et al [59] Tartally et al [65] Medina & Langmore [77] What adaptations are necessary for parasites to succeed? How do parasites differ in morphology, behaviour and physiology to non-parasites?…”

“…In this special issue, Cini et al [22] consider this for sociality, Gloag & Beekman [30] for inclusive fitness and Riehl & Feeney [14] for cooperative breeding. These studies focus on the brood parasites of social insects and/or birds, but brood-parasitic cuckoo catfish may provide new avenues for similar work if we can experimentally modify the amount of care, or paternity certainty, of cichlid host males (a point argued by Polacik et al [17] in this issue).…”

Social Recognition and Social Attraction in Group-Living Fishes

“…For instance, parent fish may 'recognize' fry or eggs within their burrow or nest as their own offspring. Given its simplicity, this mechanism can expose parents to the risk of brood parasitism (Sato, 1986;Polačik et al, 2019). However, using the same context-based mechanism, parent fish can infer from the number of cuckolders present at a spawning site the proportion of the brood they have sired, which subsequently increases or decreases the rate of filial cannibalism or parental investment (Gray et al, 2007).…”

Brood parasitism of an open‐water spawning cichlid by the cuckoo catfish

“…seem to be brood parasites. Recent studies that focused on the ecological and behavioural aspects of the brood parasitism treat the cuckoo catfish as S. multipunctatus (Blažek et al, 2018;Cohen, 2015;Cohen et al, 2018Cohen et al, , 2019Polačik et al, 2019), but exact species identification appears to have never been done in these studies.…”