Spontaneous alloparental care of unrelated offspring by non-breeding Amphiprion ocellaris in absence of the biological parents

Abstract

Many species display alloparental care, where individuals care for offspring that are not their own, but usually the behavior is contingent on the individual receiving some direct or indirect benefit. In anemonefish, after removing the breeding male, non-breeders have been observed providing care for eggs they did not sire and which are not kin. Previously this behavior was interpreted as coerced by the female. The purpose of this study was to test the alternative hypothesis that the alloparental care occurs spontaneously without prodding by the female. Groups of Amphiprion ocellaris (male, female and non-breeder) were maintained in the laboratory and behavior monitored after removing the male and both the male and female. Non-breeders began to care for eggs after male removal and further increased parental care after male and female removal. Level of care was not as high as experienced males, but additional experiments showed performance increases with experience. In a separate experiment, non-breeders were placed alone in a novel aquarium and eggs from an established spawning pair were introduced. Approximately 30% of the fish displayed extensive fathering behavior within 90 min. Taken together, our results demonstrate that fathering behavior in A. ocellaris occurs spontaneously, independent of paternity or kinship. Alloparental care, where individuals care for offspring that are not their immediate descendants occurs with reasonable frequency in nature 1-6. However, usually the behavior is actively reinforced by the breeding individuals or contingent on their presence. For instance, in the cooperative breeding cichlid, Neolamprologus pulcher, unrelated subordinates assist the dominant pair in reproduction, otherwise they would be chased out of the territory by the larger breeding pair 5,7. Similarly, in anemonefish Amphiprion clarkii, subordinate, non-breeders care for eggs they did not sire and which are not kin, and the behavior is explained as being coerced by the presence of the dominant female 8. However, anemonefish have a peculiar life history which may have provided the right context for the appearance of unconditional, spontaneous fathering behavior independent of paternity or experience. Anemonefish, or clownfish, are an iconic group of coral reef fish, beloved by the aquarium hobby, and as such their life history has been studied for decades and extensively reviewed elsewhere 9,10. Anemonefish, such as A. clarkii, and especially A. ocellaris, typically live in small groups consisting of one alpha female and one beta male which reproduce together exclusively (i.e., genetic monogamy) plus zero to several gamma non-reproductive subordinates 11,12. The reproductively suppressed gamma individuals are sexually immature 13,14. However, they can rapidly acquire male reproductive potential if the male is removed 15. These gamma individuals are tolerated by the breeding pair and maintain their own dominance hierarchy below the breeders 16. They do not normally provide care towards the eggs and are usually cha...

Alloparental care in glassfrogs: males care for unrelated clutches only when associated with their own

“…Alloparental care has been mostly studied in birds and mammals, mainly in species with complex social behaviors 56 , 57 . Thus, our study presents a novel research avenue on the costs and benefits of adoption in vertebrates with different ecological and evolutionary contexts 24 , 58 , 59 .…”

Evolution, Development and Ecology of Anemonefishes

“…as necessary during sex change as any other time, parental behavior is not expressed under natural conditions for a sex-changing fish, as they will not have offspring. However, recent research shows that even lone non-breeding fish with no parenting experience indiscriminately care for unrelated conspecific eggs in their territory (Phillips et al 2020). A recent experiment in which sex-changing fish and their partner were given eggs from another spawning pair in the colony, established the sex-changing fish as the primary caregiver of the foster eggs.…”

“…In anemonefishes, group members are unrelated and thus do not benefit from alloparental care in the traditional way via kin selection ). Yet, in some anemonefishes, when one or both parents are removed while eggs are in the nest, the non-breeder will provide care (Yanagisawa and Ochi 1986;Phillips et al 2020).…”

“…In this context, punishment by females may serve as retaliation against those who fail to care for her eggs. A second hypothesis is that alloparental care strengthens the pair bond and provides parenting experience for the mate replacement (Yanagisawa and Ochi 1986;Phillips et al 2020). Indeed, breeding experience is associated with increased male care and embryo survival Phillips et al 2020).…”

The Next Frontier in Understanding the Evolution of Coral Reef Fish Societies

“…The complex groups in which some marine fishes are organized bear many similarities with cooperatively breeding societies in mammals, birds, freshwater fishes and invertebrates (Taborsky and Limberger, 1981;Emlen, 1991;Sherman et al, 1995;Duffy et al, 2000;Bourke, 2011), but there are two key differences. First, alloparental care, where group members care for offspring other than their own, which is a feature of cooperative breeding in birds, mammals and freshwater fishes (Riedman, 1982;Wong and Balshine, 2011), has only very rarely been observed in marine fishes (see review in Wisenden, 1999;Phillips et al, 2020). However, cooperation in marine fishes may take other forms, such as subordinates modifying their growth to remain small and reduce conflict (Buston, 2003a;Wong et al, 2007), or defending and maintaining the territory (Mariscal, 1966;Iwata and Manbo, 2013).…”