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Population Structure Mediates Sexual Conflict in Water Striders

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Science  06 Nov 2009:
Vol. 326, Issue 5954, pp. 816
DOI: 10.1126/science.1180183

Abstract

Sexual conflict occurs when males and females act against each others’ interest, typically resulting in selection favoring harmful males. We performed laboratory experiments on sexual conflict that both confined individuals in isolated groups, which prevents selection acting counter to this conflict, and provided more naturalistic multigroup population structures. We show that in water striders, aggressive male mating behavior was strongly favored within groups but not favored in a multigroup population when individuals can freely disperse among groups. These observations explain the persistence of less-aggressive males within natural populations.

In social animals, exploitative strategies often create a paradox in which the most detrimental strategy for the group is also the most successful strategy for individuals within the group. This is often referred to as the tragedy of the commons, an outcome resulting from the unlimited access of individuals to a finite resource, such as herdsmen sharing a common pasture. There is always incentive for individuals to add another animal to the herd even as the commons is being overgrazed (1, 2). Although this framework is usually applied to resource consumption, it also applies to the overexploitation of females as a shared mating resource (2, 3).

Just as the overexploitation of resources can lead to local extinction, the overexploitation of females by harmful males can yield similar consequences (4). Laboratory experiments on sexual conflict often confine individuals to isolated groups. This removes the possibility that selection may counter sexual conflict as might be observed in a more natural multigroup population structure.

We measured the fitness consequences of male mating strategies in a single group versus a multigroup population where variation among groups was caused by the free movement of individuals. We tested the same individuals in both treatments, providing a demonstration of the effect of population structure on the costs and benefits of sexual conflict. The water strider Aquarius remigis provides a model species well known to engage in sexual conflict (5) and inhabit multigroup populations in streams in which individuals disperse between pools (6). Building on previous findings (3), we investigated whether the movement of females in response to local aggression creates distribution patterns of females that favor less-aggressive males in A. remigis. The experiments took place in a naturalistic laboratory environment consisting of pools that could be either isolated (no-dispersal condition) or interconnected, allowing free movement among pools (dispersal condition) (7).

When dispersal between subpools was removed, the levels of male aggression (score) and male harassment (mating attempts) were positively correlated with mating success (for aggression score, R2 = 0.723, F29 = 73.265, P < 0.001; for harassment, R2 = 0.814, F29 = 122.451, P < 0.001) (Fig. 1). Furthermore, individual aggression predicted mating success within the isolated pools (Spearman r30 = 0.893, P < 0.001), suggesting that aggression is favored within groups.

Fig. 1

Differences in mating success of aggressive males between dispersal conditions. In the dispersal condition, male aggression score (A) and harassment (B) had moderate quadratic relationship with the mating success of males. When blocking dispersal, aggression (C) and harassment (D) both strongly predicted the mating success of males.

In contrast, when dispersal was permitted, aggression only showed a modest quadratic relationship with male mating success (aggression score, R2 = 0.314, F29 = 5.492, P = 0.011; harassment, R2 = 0.254, F29 = 4.078, P = 0.030). Furthermore, females dispersed away from local aggression because mating attempts accounted for 86.4% of the variance in female dispersal between subpools (Pearson r29 = 0.930, P < 0.001). These findings indicate that free movement in a multigroup population may substantially alter costs and benefits associated with male aggression.

Sexual conflict at the scale of local social interactions is well known (8), but few studies have addressed the counterforces mediating the conflict (3, 9), examining only simple population structures. This makes local social interactions the only interactions observed while also reducing female choice. By providing a naturalistic population structure in which the free movement of individuals determines phenotypic variation within and among groups, we have observed another facet affecting mating success.

Because we used the same individuals in both conditions, we demonstrated the importance of population structure. The population structure that we provided in our experiment does not exactly replicate a natural population structure but plausibly may explain why nonaggressive males persist in natural populations despite their relative disadvantage within each and every local group.

Supporting Online Material

www.sciencemag.org/cgi/content/full/326/5954/816/DC1

Materials and Methods

References

References and Notes

  1. O. T. Eldakar, M. J. Dlugos, R. S. Wilcox, D. S. Wilson, Behav. Ecol. Sociobiol., 64, 25 (2009).
  2. Materials and methods are available as supporting material on Science Online.
  3. Funding was provided from the E. N. Huyck Preserve, the NSF Alliance for Graduate Education and the Professoriate, the Center for Insect Science, University of Arizona, NIH grant 5 K12 GM000708.
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