Exp1_hatching 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出现，普遍认为其起源于种内巢寄生（intraspecific brood parasitism）。杜鹃鲇（Synodontis multipunctatus）是目前已知唯一的专性非鸟类巢寄生生物，它寄生于坦噶尼喀湖中的口孵慈鲷，尽管其所属的歧须鮠科（Mochokidae）演化类群本身并无亲本抚育行为。杜鹃鲇会伴随寄主的产卵过程同步开展产卵行为，其卵随后会被亲代慈鲷收集并进行口孵，但寄主后续可选择性地排斥这些外来卵。关于杜鹃鲇巢寄生的起源，曾有假说认为其源于产卵过程中对慈鲷卵的捕食行为，最终使得寄主与寄生者的产卵行为在时空维度上形成匹配。本研究通过实验证实，在所有已知巢寄生生物中，杜鹃鲇具有独特的能力：可在寄主完成卵阶段拒斥后，于发育后期再次感染寄主。研究表明，杜鹃鲇幼体可在寄主的口腔腔室之外存活，并利用寄主强烈的亲本收集失散幼体的本能，在后续的口孵阶段再次感染亲代寄主。这一发现为杜鹃鲇巢寄生的演化起源提供了全新的备选假说，即寄主慈鲷的亲本抚育行为推动了该寄生策略的演化。本文属于专题议题"The coevolutionary biology of brood parasitism: from mechanism to pattern"的组成部分。