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

Abstract

Research on sociality in marine fishes is a vibrant field that is providing new insights into social evolution more generally. Here, we review the past two decades of research, identifying knowledge gaps and new directions. Two coral reef fishes, with social systems similar to other cooperative breeders, have emerged as models: the clown anemonefish Amphiprion percula and the emerald goby Paragobiodon xanthosoma. In these systems, non-breeders do not forgo their own reproduction to gain indirect genetic benefits. Rather, they do so because they stand to inherit the territory in the future and there are strong ecological and social constraints. The reasons why breeders tolerate non-breeders remain obscure, though it is plausibly a combination of weak kin selection, bet-hedging, and benefits mediated via mutualistic interactions with cnidarian hosts. The latter is particularly interesting, given the parallels with other social animals with mutualistic partners, such as acacia ants. Looking beyond the two model species, our attention is turning to species with more complex social organization, such as the damselfish Dascyllus aruanus. Here, variable group stability, conflict intensity, and reproductive skew provide opportunities to test theories of social evolution that have only been tested in a few taxa. New methods like social network analysis are enabling us to uncover more subtle effects of ecology on social interactions. More recently, comparative methods have yielded insights into the correlates of interspecific variation in sociality in the genera to which our model species belong. Phylogenetically controlled contrasts within the genus Gobiodon, have revealed the role of ecology, life history traits, and their interaction in sociality: smaller bodied species are more social than larger bodied species, which are only social on large corals. As climate change affects coral reefs, there is a pressing need to understand the many ways in which environmental disturbance influences these unique social systems. In sum, coral reef fishes have enabled us to test the robustness of current theories of social evolution in new taxa and environments, and they have generated new insights into social evolution that are applicable to a wider variety of taxa.

Evolution, Development and Ecology of Anemonefishes

“…Finally, we highlight several avenues of research that we feel are particularly exciting. This review complements a recent review of social group formation in coral reef fishes more generally (Rueger et al 2021a), going into more detail and considering social group maintenance and FIGURE 14.1 The generic anemonefish social system: a. composite photograph of a social group of the clown anemonefish Amphiprion percula in Kimbe Bay, Papua New Guinea; b. each anemonefish social group is composed of a breeding pair and a small number of non-breeders; the female is largest, the male is second largest, and the non-breeders get progressively smaller; if the female of the group dies, the male changes sex and takes the position vacated by the female. (Photo and illustration by R.…”

“…The mature male that assumes the dominant position changes sex, while the largest immature fish differentiates into a mature male to complete the breeding pair. It is believed that ecological and social constraints lie at the heart of this particular breeding strategy (Rueger et al 2021). Anemonefishes live in close association with cnidarian hosts that provide shelter from predators, food, and a refuge to lay their eggs .…”

“…Similarly, non-breeders choose to forgo reproduction and avoid the risk of moving between hosts since inheritance of the territory provides the potential for future reproduction Rueger et al 2021). Field observations in reefs of Japan have reported the presence of an individual of A. clarkii in the same anemone for 14+ years, going from subordinate immature to dominant male and subsequently changing sex to female .…”

Megacolonies: an alternative social organization in anemonefishes?

“…Social interactions and behavior of bigger social groups should be investigated in more detail, for example, using Social Network Analysis (SNA) [6,42,43]. Megacolonies could represent useful models to assess how social systems vary when ecological constraints change (in this case, change in habitat availability) and test several theories in social evolution [10].…”

“…In this clade of 28 species of Pomacentridae, scientists have developed a preliminary integrated understanding of social organization from ecological to molecular levels (reviewed in Laudet and Ravasi, 2022 [11]). Indeed, these fish, which live in mutualistic symbiosis with giant sea anemones, never abandon their host sea anemone and therefore form elaborate micro-societies that can relatively easy be studied at sea [10][11][12].…”