Social relationships in a small habitat-dependent coral reef fish: an ecological, behavioural and genetic analysis

Rueger, Theresa (2016) Social relationships in a small habitat-dependent coral reef fish: an ecological, behavioural and genetic analysis. PhD thesis, James Cook University.

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Most social animals form prolonged relationships with other individuals, whether as mating partners, parent-offspring bonds or associations with other kin. The processes that determine the strength and longevity of social relationships are often poorly understood. Many animals form monogamous breeding pairs, however, fundamental issues such as why they pair, how they choose partners and whether they mate exclusively with partners remain to be resolved. Many also live in extended family groups, but the advantages of staying or leaving family groups are complex. These issues are especially poorly understood for coral reef fishes, where social monogamy is common but appears to have evolved in species that provide either no parental care, or minimal care provided by the male. It has always been assumed that social groups in reef fish arise through strong site attachment and as a consequence of larval dispersal are not family or kin associations. In this thesis, I combined long-term behavioural observations, field experiments and new molecular tools to address these keys issues related to monogamy and genetic relatedness within social groups of a coral reef cardinalfish – Sphaeramia nematoptera (Apogonidae) in Kimbe Bay, Papua New Guinea. This species forms small, highly sedentary social groups, tends to mate in pairs within groups and is a paternal mouthbrooder. The following specific questions were addressed in the four data chapters: 1) What role does site attachment play in the choice of mates? i.e. do they primarily show allegiance to a site or a mate? 2) Are mating pairs assorted by size and which sex chooses mates?; 3) Does the social mating system reflect the genetic composition of offspring or do offspring arise from extrapair or sneak mating?; 4) Are social groups comprised of related individuals and what mechanisms might lead to kin association?

In Chapter 2, I used long term observational data to show that monogamous pairs within social groups were highly site attached compared with unpaired individuals. Following natural losses of partners or experimental mate removals, individuals rapidly formed new partnerships within the same social group rather than moving to other groups. In addition, partners did not follow their mates when they were experimentally relocated to adjacent groups, instead re-pairing with individuals within the same social group. Together, these results indicate that group cohesion is maintained through strong site attachment, and individuals show greater allegiance to sites than to mates. Thus site fidelity plays a big role in influencing pairing and pair longevity in this species.

There was strong size-assortment of males and females in pairs, with larger males pairing with larger females within social groups (Chapter 3). Size-assortative mating was not due to juvenile cardinalfish growing up together, as although individuals pair at a small size, they regularly change partners between spawning cycles until adulthood. Following natural losses, both males and females repaired with partners of more similar size than expected due to chance. Experimental removal of either males or females showed that both sexes actively choose partners, indicating that size-assortative mating was maintained by mutual mate choice.

Although most mature males and females remain paired for at least one and often several breeding cycles, genetic analysis of offspring using 19 highly polymorphic microsatellite markers revealed that both sexes exhibited extrapair mating and sneaking behaviour (Chapter 4). Multiple mothers were found in 11.4% of 105 clutches analysed, indicating that males were mouthbrooding eggs from non-partner females. Multiple paternity was found in 7.6% of clutches. The latter was unexpected, as males were thought to have limited opportunity to fertilize eggs brooded by other males. This suggests that there are males that perform sneak matings, and the high investment paternal care does not guarantee sole paternity for the brooder. Together, these results suggest that while this species is socially monogamous, both sexes will opportunistically mate with other individuals to maximize their reproductive success.

In the final chapter (5), genetic analyses revealed that individuals in social groups exhibited a higher genetic relatedness than expected on the basis of random assortment. Pairwise relatedness was 1.3 times higher within reefs than between reefs and 1.3 times higher within social groups than between social groups on the same reef. There was a negative relationship between relatedness and distance between social groups on a scale of 3.9km². High genetic relatedness within groups was explained by high levels of self-recruitment to natal reefs and an attraction among sibs, which appear to be able to settle in close proximity. While similar-sized juveniles and sub adults were more closely related when in the same social group, this same trend does not hold true for adults. This suggests an ontogenetic decline in kin attraction, possibly a mechanism to avoid inbreeding.

Overall, the results indicate that social groups of coral reef fishes are likely to be far more complex than previously anticipated. Social groups of S. nematoptera appear to arise through strong site attachment and high genetic relatedness, suggesting juveniles have a predisposition to seek out related individuals. Within social groups, strong site attachment facilitates pair formation, with both sexes having a strong preference for partners of similar size. Although pair formation may promote group stability and reproductive success, the unique paternal mouth brooding reproductive system does not preclude cheating by either males or females. Clearly, site attachment, familiarity, relatedness and opportunism all must be considered in any general model of social organization and mating systems of coral reef fishes.

Item ID: 46690
Item Type: Thesis (PhD)
Keywords: Apogonidae, assortative pairing, cardinalfish, cardinalfishes, coral reefs, dispersal, extra-pair mating, genetics, homing, matching, mate choice, microsatellite multiplex, pair formation, parentage analysis, paternal care, sexual behaviour, site attachment, site fidelity, Sphaeramia
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Rueger, Theresa, Gardiner, Naomi M., and Jones, Geoffrey P. (2014) Relationships between pair formation, site fidelity and sex in a coral reef cardinalfish. Behavioural Processes, 107. pp. 119-126.

Chapter 3: Rueger, Theresa, Gardiner, Naomi M., and Jones, Geoffrey P. (2016) Size matters: male and female mate choice leads to size-assortative pairing in a coral reef cardinalfish. Behavioral Ecology and Sociobiology, 27 (6). pp. 1585-1591.

Appendix D: Rueger, Theresa, Harrison, Hugo B., Jones, Geoffrey P., Mansour, Hicham, and Berumen, Michael L. (2015) Resolving genealogical relationships in the Pyjama cardinalfish, Sphaeramia nematoptera (Apogonidae) with 23 novel microsatellite markers. Conservation Genetics Resources, 7 (3). pp. 623-626.

Appendix E: Rueger, T., Gardiner, N.M., and Jones, G.P. (2016) Homing is not for everyone: displaced cardinalfish find a new place to live. Journal of Fish Biology, 89 (4). pp. 2182-2188.

Date Deposited: 14 Dec 2016 23:12
FoR Codes: 06 BIOLOGICAL SCIENCES > 0602 Ecology > 060205 Marine and Estuarine Ecology (incl Marine Ichthyology) @ 70%
06 BIOLOGICAL SCIENCES > 0604 Genetics > 060499 Genetics not elsewhere classified @ 30%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 100%
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