Peter M. Buston

Social hierarchies: Size and growth modification in clownfish

Conflicts of interest are part and parcel of living in a social group, although these can reduce the fitness of individual members. Here I show that clownfish (Amphiprion percula) adjust their size and growth rate according to their position in the group hierarchy, maintaining a well-defined size difference with respect to individuals above them in social rank. This strategy to prevent conflict is a surprising departure from the more usual ploy used by many animals of modifying their behaviour within the group.

The threat of punishment enforces peaceful cooperation and stabilizes queues in a coral-reef fish

Social queues, in which subordinates wait for their turn to inherit dominant breeding status, are a familiar feature of many animal societies. However, little is known about the mechanisms stabilizing social queues given the inevitable conflict over rank between group members. Here, we report the role of punishment and cooperation in promoting the stability of size-based queues in a coral-dwelling goby, Paragobiodon xanthosomus (Gobiidae). Quantitative analysis of the size-structure of queues revealed that individuals of adjacent rank differ in size by a specific size ratio, and comparisons of individual growth rates within queues demonstrated that specific size ratios are maintained over time via the regulation of subordinate growth rates. Furthermore, contest experiments demonstrated that the specific size ratio represents a threshold above which the subordinates become a threat to their immediate dominant, and as a result, dominants evict subordinates that exceed this size ratio from the group. We propose that threshold size ratios are maintained by subordinates as a form of peaceful cooperation whereby they avoid inflicting costs on dominants, and that such cooperation arises in response to the threat of punishment in the form of eviction by dominants. Societal stability is therefore achieved through the effects of punishment and cooperation acting in concert to promote the resolution of conflict over rank between group members.

Determinants of reproductive success in dominant pairs of clownfish: a boosted regression tree analysis

1. Central questions of behavioural and evolutionary ecology are what factors influence the reproductive success of dominant breeders and subordinate nonbreeders within animal societies? A complete understanding of any society requires that these questions be answered for all individuals. 2. The clown anemonefish, Amphiprion percula, forms simple societies that live in close association with sea anemones, Heteractis magnifica. Here, we use data from a well-studied population of A. percula to determine the major predictors of reproductive success of dominant pairs in this species. 3. We analyse the effect of multiple predictors on four components of reproductive success, using a relatively new technique from the field of statistical learning: boosted regression trees (BRTs). BRTs have the potential to model complex relationships in ways that give powerful insight. 4. We show that the reproductive success of dominant pairs is unrelated to the presence, number or phenotype of nonbreeders. This is consistent with the observation that nonbreeders do not help or hinder breeders in any way, confirming and extending the results of a previous study. 5. Primarily, reproductive success is negatively related to male growth and positively related to breeding experience. It is likely that these effects are interrelated because males that grow a lot have little breeding experience. These effects are indicative of a trade-off between male growth and parental investment. 6. Secondarily, reproductive success is positively related to female growth and size. In this population, female size is positively related to group size and anemone size, also. These positive correlations among traits likely are caused by variation in site quality and are suggestive of a silver-spoon effect. 7. Noteworthily, whereas reproductive success is positively related to female size, it is unrelated to male size. This observation provides support for the size advantage hypothesis for sex change: both individuals maximize their reproductive success when the larger individual adopts the female tactic. 8. This study provides the most complete picture to date of the factors that predict the reproductive success of dominant pairs of clown anemonefish and illustrates the utility of BRTs for analysis of complex behavioural and evolutionary ecology data.

Territory inheritance in clownfish

Animal societies composed of breeders and non–breeders present a challenge to evolutionary theory because it is not immediately apparent how natural selection can preserve the genes that underlie non–breeding strategies. The clownfish Amphiprion percula forms groups composed of a breeding pair and 0–4 non–breeders. Non–breeders gain neither present direct, nor present indirect benefits from the association. To determine whether non–breeders obtain future direct benefits, I investigated the pattern of territory inheritance. I show that non–breeders stand to inherit the territory within which they reside. Moreover, they form a perfect queue for breeding positions; a queue from which nobody disperses and within which nobody contests. I suggest that queuing might be favoured by selection because it confers a higher probability of attaining breeding status than either dispersing or contesting. This study illustrates that, within animal societies, individuals may tolerate non–breeding positions solely because of their potential to realize benefits in the future.

A new perspective on size hierarchies in nature: patterns, causes, and consequences.

Many plant and animal aggregations have size hierarchies within which a variety of sizes of individuals, from large to small, can be found. Size hierarchies are thought to indicate the existence of competition amongst individuals within the aggregation, but determining their exact cause is difficult. The key to understanding size hierarchies lies in first quantifying the pattern of size and growth of individuals. We conducted a quantitative investigation of pattern in the size hierarchy of the clown anemonefish Amphiprion percula, in Madang Lagoon, Papua New Guinea. Here, groups of A. percula occupy sea anemones (Heteractis magnifica) that provide protection from predators. Within each anemone there is a single group composed of a breeding pair and zero to four non-breeders. Within each group there is a single size hierarchy; the female is largest (rank 1), the male is second largest (rank 2), and the non-breeders get progressively smaller (ranks 3–6). We demonstrate that individuals adjacent in rank are separated by body size ratios whose distribution is significantly different from the distribution expected under a null model—the growth of individuals is regulated such that each dominant ends up being about 1.26 times the size of its immediate subordinate. We show that it is decisions about growth at the individual level that generate the size hierarchy at the group level, and thereby determine maximum group size and population size. This study provides a new perspective on the pattern, causes and consequences of size hierarchies.

Fasting or feasting in a fish social hierarchy

Understanding why and how subordinates of many social animals remain consistently smaller than dominants is important for determining the mechanisms underlying the structure and stability of hierarchical societies. Here we show that competition over food and conflict over social rank are ultimately responsible for the regulation of subordinate growth in the group-living reef fish, Paragobiodon xanthosomus (Gobiidae). Subordinates benefit from reducing their own food intake, and hence growth, when they approach a size where they risk conflict with dominants. Dieting appears to be a behavioural mechanism ensuring that subordinates remain smaller than dominants within the hierarchy.

Genetic relatedness in groups of the humbug damselfish Dascyllus aruanus: small, similar-sized individuals may be close kin

Kin selection plays an important role in the evolution of social behaviour in terrestrial systems. The extent to which kin selection influences the evolution of social behaviour in marine systems is largely unexplored. Generally, it is considered that kin selection is irrelevant in marine systems, because it is assumed that the dispersing larval phase of marine organisms will break up kin associations. Here, we challenge this assumption and investigate the opportunity for kin selection in a coral reef fish: the humbug damselfish Dascyllus aruanus. This fish lives in groups composed of a large male and a number of smaller females and nonbreeders. We use 10 polymorphic microsatellite loci to assess the relatedness of 265 individuals from 35 groups. The mean coefficient of relatedness among group members is 0.01 ± 0.04, suggesting that individuals are not associated with close relatives. However, the distribution of pairwise relatedness of individuals within groups has an overabundance of positive values, and indicates that there might be 35 pairs of close relatives within groups. Further analyses reveal that close relatives likely are similar in size and small in size, suggesting that they might have recruited together. We conclude that it is possible for kin selection to operate in D. aruanus, but kin recognition will be a prerequisite for such selection. This study reveals that individuals can be associated with close relatives, and there is a hidden potential for kin selection, during certain parts of the life cycle of coral reef fishes.

Patterns, causes, and consequences of marine larval dispersal

Significance Networks of marine protected areas (MPAs) have been widely implemented to combat global population declines. Although their efficacy largely depends on larval exchange between populations, quantitative analyses of dispersal have been limited due to the difficulties of tracking larvae. Here, we systematically measure dispersal in the fish Elacatinus lori, producing the first robust estimate of a dispersal kernel. We find that dispersal declines exponentially, with most larvae traveling less than 2 km from their parents. Remarkably, the distance an individual travels is unrelated to the number of days it spends in the larval phase. These results suggest that simple distance-based models may be useful conservation tools and that MPAs that are close in space will accommodate short-distance dispersers. Quantifying the probability of larval exchange among marine populations is key to predicting local population dynamics and optimizing networks of marine protected areas. The pattern of connectivity among populations can be described by the measurement of a dispersal kernel. However, a statistically robust, empirical dispersal kernel has been lacking for any marine species. Here, we use genetic parentage analysis to quantify a dispersal kernel for the reef fish Elacatinus lori, demonstrating that dispersal declines exponentially with distance. The spatial scale of dispersal is an order of magnitude less than previous estimates—the median dispersal distance is just 1.7 km and no dispersal events exceed 16.4 km despite intensive sampling out to 30 km from source. Overlaid on this strong pattern is subtle spatial variation, but neither pelagic larval duration nor direction is associated with the probability of successful dispersal. Given the strong relationship between distance and dispersal, we show that distance-driven logistic models have strong power to predict dispersal probabilities. Moreover, connectivity matrices generated from these models are congruent with empirical estimates of spatial genetic structure, suggesting that the pattern of dispersal we uncovered reflects long-term patterns of gene flow. These results challenge assumptions regarding the spatial scale and presumed predictors of marine population connectivity. We conclude that if marine reserve networks aim to connect whole communities of fishes and conserve biodiversity broadly, then reserves that are close in space (<10 km) will accommodate those members of the community that are short-distance dispersers.

Are clownfish groups composed of close relatives? An analysis of microsatellite DNA variation in Amphiprion percula

A central question of evolutionary ecology is: why do animals live in groups? Answering this question requires that the costs and benefits of group living are measured from the perspective of each individual in the group. This, in turn, requires that the groups genetic structure is elucidated, because genetic relatedness can modulate the individuals’ costs and benefits. The clown anemonefish, Amphiprion percula, lives in groups composed of a breeding pair and zero to four nonbreeders. Both breeders and nonbreeders stand to gain by associating with relatives: breeders might prefer to tolerate nonbreeders that are relatives because there is little chance that relatives will survive to breed elsewhere; nonbreeders might prefer to associate with breeders that are relatives because of the potential to accrue indirect genetic benefits by enhancing anemone and, consequently, breeder fitness. Given the potential benefits of associating with relatives, we use microsatellite loci to investigate whether or not individuals within groups of A. percula are related. We develop seven polymorphic microsatellite loci, with a number of alleles (range 2–24) and an observed level of heterozygosity (mean = 0.5936) sufficient to assess fine‐scale genetic structure. The mean coefficient of relatedness among group members is 0.00 ± 0.10 (n = 9 groups), and there are no surprising patterns in the distribution of pairwise relatedness. We conclude that A. percula live in groups of unrelated individuals. This study lays the foundation for further investigations of behavioural, population and community ecology of anemonefishes which are emerging as model systems for evolutionary ecology in the marine environment.

Does the presence of non-breeders enhance the fitness of breeders? An experimental analysis in the clown anemonefish Amphiprion percula

The stability of animal societies depends on individuals’ decisions about whether to tolerate or evict others and about whether to stay or leave. These decisions, in turn, depend on individuals’ costs and benefits of living in the group. The clown anemonefish, Amphiprion percula, lives in groups composed of a breeding pair and zero to four non-breeders. To determine why breeders accept the presence of non-breeders in this species I investigated the effect of non-breeders on multiple components of the breeders’ fitness. Non-breeders did not assist breeders in any obvious way. Experimental removal of non-breeders had no significant effect on the survival, growth, or reproductive success of breeders. Experimental removal of one of the breeding pair showed that non-breeders had little effect on the time taken for a widowed breeder to recommence breeding. The results indicate that the presence of non-breeders neither enhances, nor reduces, the fitness of breeders in A. percula. I suggest that non-breeders might modulate their effect on the fitness of breeders, either by reducing the costs they inflict or by increasing the benefits they provide, such that it just pays breeders to tolerate, rather than to evict, them. This study illustrates that animal societies can be stable even when some individuals gain nothing from the association.