Phenotypic plasticity across natural- and sexual-selection gradients in a reef fish

Walker, Stefan Peter William (2009) Phenotypic plasticity across natural- and sexual-selection gradients in a reef fish. PhD thesis, James Cook University.

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Abstract

Theory suggests that the social conditions in which an individual lives can have profound influence over which set of life history and behavioural traits are best suited for maximising expected lifetime fecundity. Variation in social system type within species is therefore hypothesised to be a major driver of the evolution of trait plasticity mechanisms. This is because those individuals that can optimise their phenotype in response to current social-based selection pressures will have an advantage over those individuals who cannot. This thesis examines the ecological and evolutionary significance of phenotypic plasticity in response to social-based selection gradients using the polygynous sex-changing reef fish Parapercis cylindrica (family Pinguipedidae). Using a combination of theoretical, discriptive and experimental procedures I tested the general hypotheses that: 1) social factors have played a significant role in the evolution of phenotypic plasticity, and that; 2) this plasticity manifests fundamental relationships between social system type, individual phenotypic expression, and the functioning and productivity of particular social groups. I address these general hypotheses by examining four aspects of P. cylindrica's evolutionary ecology: 1) social stability and conflict resolution tactics; 2) sexual selection and the sex-based modification of growth and body size; 3) sex change and the adjustment of sensory organelles, and 4) The relationships between socially facilitated life history optimisation and density dependent per capita fecundity.

Conflict over reproduction is expected in polygynous societies, both among the females who share a particular male's resources, and between males and females. The first aim of this thesis was to determine the factors promoting the stability of polygynous social groups, by examining how reproduction is apportioned among female group members and the tactics individuals employ to resolve conflict over reproductive shares. Specifically, I tested the hypotheses that: 1) polygynous males promote social stability by allocating limited sperm to larger, more dominant females, thereby minimizing intersexual conflict with the most productive sexual partners; 2) dominant females enforce disproportionate sperm allocation through the threat of subordinate-female eviction; and that 3) subordinate-females cooperate with dominant females by down-regulating gamete production in response to threatening displays. I also tested the alternative hypotheses that: 4) dominant females directly control reproduction in subordinate females, but 5) promote social stability by conceding some reproduction to subordinates as an incentive to remain peaceful in the group. Results supported hypotheses 1, 2 and 3. In addition, once a dominant female was removed from experimental groups, subordinate females were found to rapidly increased egg production. Evidence suggests that male reproductive allocation (i.e. sperm allocation), dominant-female enforcement (via the threat of attack and possible eviction), and subordinate-female cooperation (via reproductive down regulation) act together to promote social stability in P. cylindrica. This suite of conflict resolution tactics can be explained by the high reproductive rewards associated with the prospect of becoming a large dominant male (via sex change), and the advantage of maintaining a large polygynous group once the sexual transition has been made. The study illustrates that social stability and the partitioning of reproductive shares may frequently involve threeparty negotiations between social group members.

With an increase in the degree of polygyny, males must contend with greater levels of competition for the haremic male role. Essentially, the strength of sexual selection for large male body size increases with haremic group size. The second aim of this thesis was to test the hypotheses that: 1) the magnitude of sexual size dimorphism (SSD) increases with haremic group size, driving a pattern of positive sexual size allometry among social groups (i.e. Rensch's rule), and; 2) Individual adjust growth rate during sex change from female to male in response to the potential for polygyny. Larger males were found to have larger harems with larger females, and the magnitude of SSD increased with harem size. In addition, experimental fishes were found to increase growth rate in response to polygyny potential during sex change. Thus, evidence suggests that sexual selection for male body size is the ultimate cause of variation in growth rate, and variation in growth rate is the proximate cause of sexual size allometry. The study provides compelling evidence in support of the sexual selection hypothesis for Rensch's rule, and highlights the importance of growth modification in the shaping of morphological patterns in nature.

The growth and morphology of the organelles associated with the detection of sound and movement (i.e. otoliths) are highly conservative in fishes and finely tuned to specific habitat and life-style requirements. However, changes in behaviour and use of space typically occur coincident with sexual transition. This means that the optimal configuration of the sensory apparatus may also change, driving a selection pressure for the readjustment of sensory organelles (i.e. otoliths). The third aim of this thesis was to test the hypothesis that otolith growth and morphology is modified during sex change. Manipulative experiments illustrated that otolith discontinuities are formed during the course of sex change, characterised by a shift in the primary growth axis and a shift in microstructural density. In addition, the larger the harem the sex-changer inherited and defended, the greater the shift in otolith growth and morphology. These data suggest that sex-changing individuals may adjust their sensory apparatus so as to optimise life history in accordance with their new reproductive mode. However, the confirmation of this functional hypothesis will require further studies using an eco-physiological approach. Nonetheless, the discovery of sex-change associated otolith discontinuities represents a novel and powerful tool in fish and fisheries science. Since otolith growth is characterised by the accretion of daily bands, sex-change associated otolith signatures provide a means to detect the precise age at sex change. This will allow the life history of sex-changing fishes to be examined at a resolution not previously possible.

Positive density dependence (i.e. the Allee effect; AE) often has important implications for the dynamics and conservation of populations. The final aim of this thesis was to examine the interplay between density dependent sex ratio adjustment and the AE. Specifically, using an analytical model I show that an AE is expected whenever one sex is more fecund than the other and sex ratio bias towards the least fecund sex increases with density. I then illustrate the robustness of this pattern, using Monte Carlo simulations, against a range of body size-fecundity relationships and sex allocation strategies. Finally, I test the model using the sex-changing polygynous reef fish Parapercis cylindrica; positive density dependence in the strength of sexual selection for male size is evidenced as the causal mechanism driving local sex ratio adjustment, hence the AE. Model application may extend to invertebrates, reptiles, birds and mammals, in addition to 70+ reef fishes. I suggest that protected areas may often outperform harvest quotas as a conservation tool, since the latter promotes population fragmentation, reduced polygyny, a balancing of the sex ratio and hence up to a 50% decline in per capita fecundity, while the former maximises polygyny and source-sink potential

Taken together, the results of this thesis showcase the extent to which individuals modify their traits in response to social-based natural- and sexual-selection pressures, and the fundamental role that phenotypic plasticity plays in driving ecological patterns and processes.

Item ID: 29238
Item Type: Thesis (PhD)
Keywords: Parapercis cylindrica; phenotypic plasticity; social system; reef fish; reproduction; growth; conflict resolution; life history; sexual size dimorphism; otolith signatures
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Publications arising from this thesis are available from the Related URLs field. The publications are:

Walker, Stefan P.W., and McCormick, Mark I. (2009) Sexual selection explains sex-specific growth plasticity and positive allometry for sexual size dimorphism in a reef fish. Proceedings of the Royal Society of London Series B, Biological Sciences, 276 (1671). pp. 3335-3343.

Walker, Stefan P.W., and McCormick, Mark I. (2009) Fish ears are sensitive to sex change. Biology Letters, 5 . pp. 73-76.

Munday, P. L., Ryen, C.A., McCormick, M. I., and Walker, S.P.W. (2009) Growth acceleration, behaviour and otolith check marks associated with sex change in the wrasse Halichoeres miniatus. Coral Reefs, 28 (3). pp. 623-634.

Frisch, A.J., Walker, S.P.W., McCormick, M.I., and Solomon-Lane, T.K. (2007) Regulation of protogynous sex change by competition between corticosteroids and androgens: an experimental test using sandperch, Parapercis cylindrica. Hormones and Behavior, 52 (4). pp. 540-545.

Walker S.P.W., and C. Ryen. (2007) Opportunistic hybridization between two congeneric tropical reef fish. Coral reefs, 26(3). pp. 539.

Walker, Stefan P.W., and McCormick, Mark I. (2004) Otolith-check formation and accelerated growth associated with sex change in an annual protogynous tropical fish. Marine Ecology Progress Series, 266 . pp. 201-212.

Walker, S.P.W., Ryen, C.A., and McCormick, M.I. (2007) Rapid larval growth predisposes sex change and sexual size dimorphism in a protogynous hermaphrodite, Parapercis snyderi Jordan & Starks 1905. Journal of Fish Biology, 71 (5). pp. 1347-1357.

McCormick, Mark I., Ryen, Christopher A., Munday, Philip L., and Walker, Stefan P.W. (2010) Differing mechanisms underlie sexual size-dimorphism in two populations of a sex-changing fish. PLoS ONE, 5 (5). 1- 8.

Date Deposited: 24 Oct 2013 02:32
FoR Codes: 06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060304 Ethology and Sociobiology @ 33%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060201 Behavioural Ecology @ 34%
06 BIOLOGICAL SCIENCES > 0603 Evolutionary Biology > 060307 Host-Parasite Interactions @ 33%
SEO Codes: 97 EXPANDING KNOWLEDGE > 970106 Expanding Knowledge in the Biological Sciences @ 100%
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