Exp3_acceptance from Parasitic cuckoo catfish exploit parental responses to stray offspring

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’.

种间巢寄生（interspecific brood parasitism）在鸟类与社会性昆虫的多个独立演化支系中均有发生，其演化被推测起源于种内巢寄生（intraspecific brood parasitism）。杜鹃鲶（Synodontis multipunctatus）是目前已知唯一的专性非鸟类巢寄生生物，尽管其所属的鮡科（Mochokidae）演化支系并无育幼行为，但它仍寄生于坦噶尼喀湖（Lake Tanganyika）的口育慈鲷（mouthbrooding cichlid）。杜鹃鲶会参与宿主慈鲷的产卵活动，其鱼卵随后会被亲代慈鲷收集并纳入口腔育幼，但宿主后续也可能选择性排斥这些外来鱼卵。关于杜鹃鲶巢寄生的起源，有假说认为其源自产卵过程中对慈鲷鱼卵的捕食行为，最终使得宿主与寄生生物的产卵行为在空间与时间上达成匹配。本研究通过实验证实，在所有已知的巢寄生生物中，杜鹃鲶的独特之处在于：即便宿主已将其鱼卵排斥，它仍能在发育后期再次感染宿主。研究表明，杜鹃鲶幼体可在宿主口腔腔外存活，并利用宿主强烈的育幼本能——即收集失散幼体的行为——在后续的育幼阶段再次感染亲代宿主。这一发现为杜鹃鲶巢寄生的演化起源提供了新的解释路径：宿主慈鲷的育幼反应推动了该寄生行为的演化。本文属于主题刊《巢寄生的协同演化生物学：从机制到模式》（The coevolutionary biology of brood parasitism: from mechanism to pattern）的组成部分。