Sexual conflict and environmental change

c⃝ Indian Academy of Sciences

RESEARCH ARTICLE

Sexual conflict and environmental change: trade-offs within and between the sexes during the evolution of desiccation resistance

LUCIA KWAN1,2, STÉPHANIE BEDHOMME1,3, N. G. PRASAD1,4 and ADAM K. CHIPPINDALE1∗

1Department of Biology, Queen’s University, Kingston, Ontario K7L 3N6, Canada 2Present address: Department of Biology, University of Ottawa, Ottawa, Ontario KIN 6N5, Canada

3Present address: University of Muenster, Institute for Evolution and Biodiversity, Animal Evolutionary Ecology Group, Huefferster. 1, D-48149 Muenster, Germany

4Present address: Indian Institute of Science Education and Research, Salt Lake City, Kolkata 700 106, India

Abstract

Intralocus sexual conflict occurs when males and females experience sex-specific selection on a shared genome. With several notable exceptions, intralocus sexual conflict has been investigated in constant environments to which the study organisms have had an opportunity to adapt. However, a change in the environment can result in differential or even opposing selection pressures on males and females, creating sexual conflict. We used experimental evolution to explore the interaction between intralocus sexual conflict, sexual dimorphism and environmental variation in Drosophila melanogaster. Six populations were selected for adult desiccation resistance (D), with six matched control populations maintained in parallel (C). After 46 gener- ations, the D populations had increased in survival time under arid conditions by 68% and in body weight by 20% compared to the C populations. The increase in size was the result of both extended development and faster growth rate of D juveniles. Adaptation to the stress came at a cost in terms of preadult viability and female fecundity. Because males are innately less tolerant of desiccation stress, very few D males survived desiccation-selection; while potentially a windfall for survivors, these conditions mean that most males’ fitness was determined posthumously. We conjectured that selection for early maturation and mating in males was in conflict with selection for survival and later reproduction in females. Consistent with this predic- tion, the sexes showed different patterns of age-specific desiccation resistance and resource acquisition, and there was a trend towards increasingly female-biased sexual size dimorphism. However, levels of desiccation resistance were unaffected, with D males and females increasing in parallel. Either there is a strong positive genetic correlation between the sexes that limits independent evolution of desiccation resistance, or fitness pay-offs from the strategy of riding out the stress bout are great enough to sustain concordant selection on the two sexes. We discuss the forces that mould fitness in males under a regimen where trade-offs between survival and reproduction may be considerable.

[Kwan L., Bedhomme S., Prasad N. G. and Chippindale A. K. 2008 Sexual conflict and environmental change: trade-offs within and between the sexes during the evolution of desiccation resistance. J. Genet. 87, 383–394]

Introduction Sexual conflict arises when the fitness interests of males and females differ. There are two distinct forms of con- flict, depending upon whether there is direct physical coer- cion (interlocus) or genetic constraint on sex-specific evolu- tion (intralocus). Interlocus sexual conflict occurs when a locus expressed in one sex reduces the fitness of the opposite sex through direct physical interaction (e.g., harassment and

*E-mail: chippind@queensu.ca.

toxicity). This selects for the expression in the opposite sex, at other loci, of a counteracting mechanism that will reduce the fitness costs of sexual interaction. This form of con- flict may contain the ingredients for an arms race (or evo- lutionary chase) between the sexes driven by sexually antag- onistic coevolution (Parker 1979; Rice 1998). An apparent example of this dynamic is seen in the evolution of elabo- rate grasping (males) and anti-grasping (females) structures in the gerrid water striders (Rowe and Arnqvist 2002). Nu- merous other examples have recently been catalogued, sug-

Keywords. desiccation resistance; Drosophila melanogaster; environmental variation; experimental evolution; intersexual genetic corre- lation; intralocus sexual conflict.

Journal of Genetics, Vol. 87, No. 4, December 2008 383

Lucia Kwan et al.

gesting that interlocus sexual conflict is both taxonomically widespread and occurs through a variety of different organs of expression (Arnqvist and Rowe 2005).

The second form of conflict, intralocus sexual conflict, is likely to prove equally pervasive but is less apparent. In- tralocus sexual conflict arises because males and females ex- perience sex-specific selection on a shared genome. This creates conflict when the same allele or expression pattern has opposite effects on the relative fitness of each sex, lead- ing to a kind of tug-of-war over gene expression between males and females (Rice and Chippindale 2001). Without the evolution of mechanisms to isolate female selection from male selection, the outcome is genotypes that are optimized for neither sex and a reduction in average fitness (Rice and Chippindale 2002). Chippindale et al. (2001) and Prasad et al. (2007), showed evidence for intralocus sexual conflict in Drosophila melanogaster in a strong and negative intersexual genetic correlation for adult fitness. The genotypes that code for high fitness females tended to code for low fitness males and vice versa. Since then, a methodologically and taxonom- ically broad canon of results has come to light, including fur- ther data from D. melanogaster, other insects, reptiles and amphibians, and mammals, including humans (Bedhomme and Chippindale 2007).

Because the sexes themselves represent different envi- ronments for gene expression, intralocus sexual conflict sug- gests a mechanism through which genetic variation for fit- ness traits may be maintained in populations, even under con- stant external environmental conditions (Rice 1984; Gibson et al. 2002). However, the interactions between sexual con- flict, sexual dimorphism and external environmental varia- tion may have important consequences that have been largely overlooked until now. A change in the environment can re- sult in differential or even opposing selection pressures on males and females, and this is particularly likely when the sexes are dimorphic. This is because extant sexual dimor- phism may not dictate the same best response to the same new external selective agent by both sexes. For example, an environmental stress that makes it beneficial to migrate for one sex—the more mobile sex—may not create condi- tions that favour migration in the other sex, where the cost of movement is greater, along with the odds of survival in situ (Perrin and Mazalov 2000; Munshi-South 2008). Numerous examples could be imagined, particularly involving sexual size dimorphism (SSD) and environmental change. While sex-specific expression and dimorphism represent cures for intralocus sexual conflict, a changing environment has the potential to induce new forms of sexual antagonism. D. melanogaster is a good model to study the interplay

between sexual conflict and adaptation to a novel environ- ment. The species is promiscuous and sexually dimorphic, with males being smaller and slower growing than females, and they are legendarily responsive to selection. In one of the few studies linking sexual conflict to adaptation in a new environment, Chippindale et al. (1998) discussed sex-

specific selection on the life-history and physiology of D. melanogaster selected for desiccation tolerance. They noted that the sex-specific patterns of adaptation to stress were linked to initial sexual dimorphism in body size and develop- ment time, along with different resource acquisition and allo- cation priorities. Different and opposing selection pressures for males and females apparently resulted from the same en- vironmental challenge.

As is typical of small organisms, drosophilids are inher- ently sensitive to desiccation because of a high surface area to volume ratio. However, they have undergone multiple adap- tive radiations in arid regions and their adaptation to desicca- tion has been widely studied in both nature (e.g., Marron et al. 2003; Matzkin et al. 2007) and the laboratory (e.g., Hoff- mann and Parsons 1989; Gibbs et al. 1997; Chippindale et al. 1998). In the laboratory, it has been found that the evo- lution of desiccation resistance in Drosophila can result in a complex and extensive reshaping of their phenotype and life-history. Prasad and Joshi (2003) noted that desiccation resistance is reliably associated with changes in two adult life-history traits, longevity and fecundity. Previous studies showed that adult populations of D. melanogaster selected for desiccation resistance showed increased mean longevity and reduced early fecundity (Hoffmann and Parsons 1989; Rose et al. 1990, 1992; Leroi et al. 1994a,b), suggesting that the strong genetic correlations between these traits generate trade-offs and influence the response to selection.

Chippindale et al. (1998) found similar age-related pat- terns of desiccation resistance and resource management in males and females of control populations, but not in males and females of desiccation-selected populations. In the lat- ter populations, females showed greater desiccation resis- tance associated with markedly higher rates of carbohydrate and bulk water storage as larvae and young adults than both control populations and desiccation-selected males. To un- derstand the sex-specific selection pressures underlying this differentiation, a closer look at the experimental protocol is necessary. Young adult flies were subjected to an intense desiccation period (low to zero relative humidity) every gen- eration, after having grown and lived in relatively rich food, with…