The evolution of sociality in
habitat-specialist coral reef
fishes
Source: http://www.ultimatereef.net/forums/showthread.php?t=362748 accessed 29/9/13
Faculty of Science, Medicine and Health
School of Biological Sciences
A project proposal submitted in partial fulfilment of the requirements for the degree of Doctor of
Philosophy
2013
Abstract
One of the most astonishing facets of animal societies is the decision of individuals to join a group as
a non-breeding subordinate member. This decision is intriguing as, on the face of it, one might
expect an individual to maximise its genetic contribution by breeding as soon as possible and as
many times as possible for the duration of its life. Why then, do we observe so many examples in
nature, including our own species, in which individuals routinely delay or completely forgo their own
reproductive opportunities in order to join and remain within a group? The fact that this behaviour
has been shown to vary considerably, within a single species and also between multiple species
across genera or families, indicates that there may be external factors influencing the behaviour.
This project will investigate the ecological, social and life history factors at the root of this decision in
a model group of coral-reef associated fishes. Using cooperative breeding theory as an overarching
framework, I will combine broad phylogenetic comparisons of these key factors with manipulative
field experiments across a broad geographic range to assess the causal links between these factors
and the formation of stable groups. This project will greatly advance our understanding of the
generality of cooperative breeding theory as an explanation for the evolution of sociality, which has
proven to be one of the key challenges in the field of evolutionary biology. Understanding the role
these factors have played in the evolution of sociality is valuable as it provides insights into how
these societies will react to varying environmental conditions in the future. Such predictions are
becoming increasingly important in a period of intensifying global environmental change.
1
Introduction
The animal kingdom contains many examples of species, including our own, which form surprisingly
complex social structures (Munday et al., 1998, Purcell, 2011, Grueter et al., 2012, Johnson et al.,
2013, Chapais, 2013). The size, structure and composition of these groups can vary both within and
between species, from a pair of monogamous individuals (Kleiman, 2011, Servedio et al., 2013) to
large and highly complex societies exhibiting social hierarchies (Duffy and Macdonald, 2010, Nandi
et al., 2013). Such immense variation in social structure is intriguing as it suggests that there may be
underlying social, ecological or life history factors that influence the evolution of stable groups and
their maintenance over many generations.
One of the most fascinating aspects of sociality is the tendency of individuals to delay or forgo their
own reproductive opportunities in order to join or remain within a group (Buston, 2003, Faulkes and
Bennett, 2013, Margraf and Cockburn, 2013). The reasons for this decision are not universally clear
despite being the focus of many behavioural studies (Emlen, 1994, Cockburn, 1996, Arnold and
Owens, 1998, Hatchwell and Komdeur, 2000, Pen and Weissing, 2000, Buston and Balshine, 2007).
Notwithstanding the excellent work conducted in this field, a general explanation for the reasons
that non-breeders choose to forego their own reproductive opportunities and remain within a group
is still lacking. One hindrance to the resolution of this problem is that there have been relatively few
studies examining social group living in taxa besides birds, mammals and insects (but see Wong and
Buston (2013)). This limited taxonomic scope greatly impairs our ability to assess the universality of
frameworks of social evolution.
One of the most promising frameworks within which to study this phenomenon is Cooperative
Breeding theory (Brown, 1974), which describes a social system in which non-breeding subordinate
members assist breeding members of the group to raise offspring. Cooperative Breeding theory
encompasses several hypotheses to explain individual decisions that may lead to sociality (Table 1).
Some of these hypotheses, such as the life history hypothesis (Rowley and Russell, 1990), examine
intrinsic factors of the individuals which may act to predispose them to cooperative breeding and
sociality, while other theories such as the ecological constraints hypothesis (Emlen, 1982) investigate
extrinsic factors which may prohibit the dispersal of individuals, leading to sociality. These
hypotheses are not mutually exclusive and often act in concert with each other to promote the
formation of stable groups (Hatchwell and Komdeur, 2000).
The vast majority of studies that have focused on testing the four key hypotheses of cooperative
breeding theory (Table 1) have done so using broad phylogenetically controlled comparisons of
relevant ecological, social and life history variables in birds, mammals and insects (Cockburn, 1996,
Arnold and Owens, 1998, Johnson et al., 2002, Purcell, 2011). In other words, such studies attempt
to investigate the evolution of sociality by seeking differences in traits between multiple social and
asocial species within a given lineage. While broad generalisations can be made from such contrasts,
conclusions regarding the causality of effects cannot be confidently made. In contrast, other studies
have addressed these hypotheses through refined experimental manipulation, thus demonstrating
causality, but have been focused on just one or a few species which reduces the ability to draw
general conclusions (Wong et al., 2008). The combination of these approaches holds the potential to
provide an insight into the generality and causality of sociality across a broad range of species.
2
Table 1: Four of the major hypotheses contributing to the Cooperative Breeding Theory and key factors thought to influence the respective hypotheses.
Hypothesis
Description
Key Factors
Key Predictions
Key References
Ecological
Explains how the costs of dispersing due Coral size, distance
Emlen (1982)
 Increase in ecological constraints
Constraints
to ecological pressures such as high
between corals,
should promote sociality in asocial
predation rates or low resource
habitat saturation
species.
availability may make it more
 Decrease in ecological constraints
preferable for an individual to delay its
should promote asociality in social
dispersal and thereby refrain from
species.
independent breeding.
Life History
Describes how life history traits of a
species or lineage, such as low fecundity
and low mortality rates, could lead to
habitat saturation and a shortage of
suitable breeding sites which may
predispose a species or lineage to
social group-living.
Reproductive output, 
life span

Benefits of
Philopatry
Focuses of the benefits of remaining on
the natal site, thereby promoting
sociality. These benefits are often in the
form of gaining access to high quality
habitat following the death of dominant
individuals where there is high variation
in habitat quality.
Habitat size, habitat
variability, habitat
saturation, life span,
fecundity

Examines the social reasons behind a
dominant’s decision to allow the
presence of subordinate individuals.
Sociality may arise when the costs to
dominant individuals of expelling
subordinates from the territory are high
or where the subordinates provide a
fitness benefit (e.g. caring for offspring)
to the dominant individuals.
Reproductive output
with/without
subordinates
present.

Breeder
Tolerance



Social species characterised by
lower mortality and fecundity.
Asocial species characterised by
greater mortality and fecundity.
Rowley and Russell (1990);
Arnold and Owens (1998);
Hatchwell and Komdeur (2000)
Social species will live in
environments with high variance in
habitat quality.
Asocial species will live in
environments where habitat quality
is less variable.
Stacey and Ligon (1991)
Presence of non-breeders in a social
species will have a neutral or
positive impact on breeder fitness.
Breeders in social species
experience greater cost of expelling
non breeders.
Presence of non-breeders in an
asocial species will have a negative
impact on breeder fitness.
Kokko et al.(2001)
3
The use of cooperative breeding theory to identify the factors influencing sociality may not only
provide insights into the evolution and maintenance of group-living, but may also enable us to make
predictions about how societies may change under varying social and environmental conditions. An
effective method of examining the effects that large scale environmental variations can have on
sociality is to conduct studies of sociality across multiple geographic locations. For example, since
temperature is more stable at lower latitudes than higher latitudes (Tewksbury et al., 2008),
ecological factors linked to temperature, such as habitat quality, resource availability or
precipitation, would likely follow a similar pattern of lower variation towards lower latitudes and
higher variation towards higher latitudes. These environmental influences could in turn have an
effect on the decisions of subordinates about whether to join a group or disperse (Rubenstein and
Lovette, 2007, Jetz and Rubenstein, 2011). Purcell (2011) reviewed social systems in terrestrial
arthropods and found that within families and even within species, that many arthropods tend to
show a higher degree of sociality at lower latitudes than at higher latitudes. Cross-latitudinal
investigations of sociality have also been conducted on bees (Cronin and Schwarz, 1999), spiders
(Riechert and Jones, 2008), bats (Johnson et al., 2013) birds (Jetz and Rubenstein, 2011) and badgers
(Johnson et al., 2002) among others. However, there appears to be a relative paucity of similar
studies in other taxa, including those living in the marine environment. Such studies would be
valuable for increasing our understanding of the evolution of sociality especially since marine species
have been shown to differ markedly to terrestrial species in metrics such as thermal tolerance across
latitudes (Sunday et al., 2011).
Habitat specialist reef fishes are one group of marine fishes with enormous potential for testing
hypotheses of cooperative breeding theory (Herler et al., 2011, Wong and Buston, 2013). In
particular, species from the genera Gobiodon and Paragobiodon, are excellent candidates with
which to perform both phylogenetically controlled contrasts and experimental manipulations, as
they are ubiquitous on coral reefs (Herler et al., 2011) and are socially extremely diverse (Herler et
al., 2009, Thacker and Roje, 2011, Duchene et al., in press). Further, the fact that they reside within
discrete patches of coral means that experimental manipulations of ecological parameters are
logistically simple (Munday and Wilson, 1997, Munday, 2001). Individuals within corals can also be
tagged using a fluorescent elastomer so that the same individuals can be recognised over time
(Malone et al., 1999), enabling longer term field assessments. There are at least 26 species in the
genus Gobiodon (Duchene et al., in press) and at least five species in the genus Paragobiodon
(Froese and Pauly, 2011, OzFishNet, 2012) which display a variety of social organisations ranging
from obligate pair forming, (such as G. histrio (Munday et al., 1998)), to group living with a single
breeding pair (such as P. xanthosoma (Wong et al., 2008)) to group living with multiple breeding
individuals (such as G. Quinquestrigatus (Thompson et al., 2007)).
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The overall goal of the current study is to combine a broad phylogenetic comparative approach
with finer scale experimental investigations to test the generality of cooperative breeding theory
as an explanation of social system diversity, using habitat-specialist coral reef fishes as a model
system. The combination of these techniques to test hypotheses using a relatively under-studied
group of organisms will provide great insight into the evolutionary origins and maintenance of social
behaviour. To achieve this goal, I will break down the investigation into the following testable aims:
1) Conduct a broad phylogenetic comparison of sociality among a socially diverse group of
coral reef associated fishes from the genera Gobiodon and Paragobiodon.
2) Conduct comparative field observations of pairs of congeneric social and asocial Gobiodon
and Paragobiodon species across a latitudinal gradient, to test whether key factors
(identified through the phylogenetic comparison) are related to variation in sociality and
whether these variations change across latitudes.
3) Conduct experimental manipulations of these key factors using pairs of congeneric social
and asocial Gobiodon and Paragobiodon species across a latitudinal gradient, to provide
causal support for the role of these factors in the evolution of sociality.
The outcomes of this study will identify and expose the causal links between the key ecological,
social factors and life history factors and sociality, and thereby represent cutting edge research
in the field of evolutionary biology and behavioural ecology. Knowledge of the role that such
factors play in influencing sociality will also be relevant for predicting how societies will respond
to varying environmental conditions, especially during this period of increasingly variable
environmental conditions.
5
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