Update
TRENDS in Ecology and Evolution
male offspring are greater than the male-imposed reduction in her own reproduction; under some conditions, female susceptibility to males can be advantageous [4,5]. Chapman et al. argue that such ‘indirect benefits [to the female] are expected to be a weak force in the face of direct selection on preference’, but cite only a theoretical model as evidence. The track record of quantitative conclusions based on mathematical models of sexual selection is rather dismal [2]. Recall, for instance, the now discarded dogma that Fisherian female choice was unlikely because quantitative models had ‘proven’ that there is little or no heritable variability for sexually selected traits in males. The conflicting demonstrations regarding the feasibility of handicap models constitute another example. In addition, empirical evidence indicates that indirect benefits to the female are not necessarily small [6]. Thus, the studies that Chapman et al. cite as documenting the overall cost of manipulation for females, none of which took this possible indirect benefit into account, fail to demonstrate a net cost rather than a net benefit. A second weakness is that costs and benefits cited by Chapman et al. were measured under captive rather than field conditions. It is trite, but nevertheless true [4], that fitness measures made in captivity do not reliably document selection in nature. For instance, reductions in female lifespan in the lab [7] might be irrelevant in nature if females die at earlier ages under natural conditions. Ecological realism is especially important for traits possibly involved in male– female conflict [1], because the demonstration of conflict depends on precise quantitative balancing of costs and benefits. Finally, Chapman
Vol.18 No.9 September 2003
439
et al. do not discuss morphological evidence from many other species that speaks strongly against the importance of new male– female conflict models [8 – 11]. References 1 Chapman, T. et al. (2003) Sexual conflict. Trends Ecol. Evol. 18, 41 – 47 2 Andersson, M. (1994) Sexual Selection, Princeton University Press 3 Eberhard, W.G. (2002) Female resistance or screening? Male force versus selective female cooperation in intromission in sepsid flies and other insects. Rev. Biol. Trop. 50, 485– 505 4 Cordero, C. and Eberhard, W.G. (2003) Female choice of antagonistic male adaptations: a critical review of some current research. J. Evol. Biol. 16, 1 – 6 5 Kokko, H. (2001) Fisherian and ‘good genes’ benefits of mate choice: how (not) to distinguish between them. Ecol. Lett. 4, 322 – 326 6 Møller, A.P. and Jennions, M. (2001) How important are direct fitness benefits of sexual selection? Naturwissenschaften 88, 401– 415 7 Chapman, T. et al. (1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373, 241 – 244 8 Eberhard, W.G. (1985) Sexual Selection and Animal Genitalia, Harvard University Press 9 Eberhard, W.G. (2001) The functional morphology of species-specific clasping structures on the front legs of male Archisepsis and Palaeosepsis flies (Diptera, Sepsidae). Zool. J. Linn. Soc. 133, 335 – 368 10 Huber, B.A. (1998) Spider reproductive behaviour: a review of Gerhardt’s work from 1911 – 1933, with implications for sexual selection. Bull. Br. Arachnol. Soc. 11, 81 – 91 11 Eberhard, W.G. (1997) Sexual selection by cryptic female choice in insects and arachnids. In Evolution of Mating Systems in Insects and Arachnids (Choe, J.C. and Crespi, B.J., eds), pp. 32– 57, Cambridge University Press
0169-5347/$ - see front matter q 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0169-5347(03)00180-0
Sexual conflict Alex Co´rdoba-Aguilar and Jorge Contreras-Gardun˜o Instituto de Ecologı´a, Universidad Nacional Auto´noma de Me´xico, Apdo. Postal 70-275, Circuito exterior Ciudad Universitaria 04510, Mexico, D.F.
Current positions have redefined the evolution of courtship traits as the takeover of reproductive decisions of one sex by the other sex, giving rise to an unending coevolution, in which one sex (predominantly males) sets the scene (given that selection for siring offspring is frequently stronger in males than in females [1 –3]). Chapman et al. [3] argue that such sexual conflict is the underlying force during sexual interactions and that males, at the fitness expense of females, usually emerge at the forefront of the coevolutionary race. We perceive two problems with their review and its implications: (1) the evidence that could reject the alternative hypothesis of traditional female choice is still inconclusive. This results from a lack of predictions that can disentangle the hypothesis of traditional female choice from that of sexual
Corresponding author: Alex Co´rdoba-Aguilar (
[email protected]). http://tree.trends.com
conflict; and (2) extreme generalizations of a widespread nature of sexual conflict. The sexual conflict hypothesis predicts that females become a target of male manipulation that results in mating. Given this, one can be mislead and easily interpret ‘aggressive’ male traits as a consequence of sexual conflict, even when these traits are also predicted by traditional female choice, with females gaining highly successful sons in spite of being ‘harmed’ by their mates [2,4]. Lamentably, no studies have separated both hypotheses because no measurements have been collected of direct and indirect benefits for females mated to males differing in their degree of ‘aggressive’ traits to establish female net fitness payoffs [4]. There are three additional approaches for unraveling both positions. The first is to investigate female reproductive traits involved in fertilization. In spite of being repeatedly claimed as an
Update
440
TRENDS in Ecology and Evolution
important issue both theoretically and experimentally [5], researchers ignore how female reproductive traits intervene during fertilization. Once this is clarified, we can then ascribe female traits as ‘resistant’ or ‘selective’. The second is to study the genetics of the female preference and associated male traits [5]. A genetic correlation is expected between both traits only if traditional female choice is occurring. The third and final approach is to track the rates of origin of female and male traits on phylogenies once resistance or selectivity has been determined. This will explain the prevalence of either process. Studies of fruit flies and water striders have suggested that negative fitness outcomes for females are a widespread phenomenon, but it is premature to claim that sexual conflict is widespread based on data from relatively few taxa. Related to this, no discussion was made by Chapman et al. of recent studies showing how females control both their reproductive decisions and the fitness payoffs accrued by them (e.g. [6 – 10]). By omitting them, readers might not only believe that the dichotomy of sexual conflict and female choice does not exist, but, if it did, that it has been settled in favour of sexual conflict.
Vol.18 No.9 September 2003
References 1 Holland, B. and Rice, W.R. (1997) Chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52, 1 – 7 2 Parker, G.A. (1979) Sexual selection and sexual conflict. In Sexual Selection and Reproductive Competition in Insects (Blum, M.S. and Blum, N.A., eds), pp. 123– 166, Academic Press 3 Chapman, T. et al. (2003) Sexual conflict. Trends Ecol. Evol. 18, 41 – 47 4 Cordero, C. and Eberhard, W.G. (2003) Female choice of sexually antagonistic male adaptations: a critical review of some current research. J. Evol. Biol. 16, 1 – 6 5 Simmons, L.W. (2001) Sperm Competition and its Evolutionary Consequences in the Insects, Princeton University Press 6 Edvardsson, M. and Arnqvist, G. (2000) Copulatory courtship and cryptic female choice in the red flour beetles Tribolium castaneaum. Proc. R. Soc. Lond. Ser. B 267, 559 – 563 7 Elgar, M.A. et al. (2000) Female control of paternity in the sexually cannibalistic spider Argiope keyserlingi. Proc. R. Soc. Lond. Ser. B 267, 2439–2443 8 Sakaluk, S.K. and Eggert, A-K. (1996) Female control of sperm transfer and intraspecific variation in sperm precedence: antecedents to the evolution of a courtship food gift. Evolution 50, 694 – 703 9 Tallamy, D.W. et al. (2002) Male traits under cryptic female choice in the spotted cucumber beetle (Coleoptera: Chrysomelidae). Behav. Ecol. 13, 511–518 10 Tallamy, D.W. et al. (2003) Copulatory courtship signals male genetic quality in cucumber beetles. Proc. R. Soc. Lond. Ser. B 270, 77 – 82 0169-5347/$ - see front matter q 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0169-5347(03)00182-4
| Letters Response
Response to Eberhard and Cordero, and Co´rdoba-Aguilar and Contreras-Gardun˜o: sexual conflict and female choice Tracey Chapman1, Goran Arnqvist2, Jenny Bangham1 and Locke Rowe3 1
Department of Biology, University College London, Darwin Building, Gower Street, London, UK WC1E 6BT Department of Animal Ecology, Evolutionary Biology Centre, University of Uppsala. Norbyva¨gen 18d, SE - 752 36 Uppsala, Sweden 3 Department of Zoology, University of Toronto, 25 Harbord St. Toronto, ON, Canada M5S 3G5 2
Eberhard and Cordero [1] begin with a claim that, in our recent TREE article [2], we are inconsistent in our use of an older, and new narrower definition of sexual conflict. For the former, we quoted the original views of Parker, Trivers, and Dawkins, and we stand by this usage. The ‘narrow’ definition noted by Eberhard and Cordero was not a definition at all, but rather an attempt to set recent models of sexual conflict into the broader context of sexual selection theory (direct versus indirect selection, and their signs). Co´rdoba-Aguilar and Contreras-Gardun˜o [3] imply that we ignore difficulties in disentangling sexual conflict from ‘traditional models’. In fact, we were clear that the ‘boundary, if there is one, between traditional models of sexual selection and sexual conflict has not yet been carefully explored theoretically’ [2]. Yet, we believe that there is much to learn along this road, and initial forays
Corresponding author: Locke Rowe (
[email protected]). http://tree.trends.com
have supported this view. Eberhard and Cordero consider this an overly optimistic viewpoint. Eberhard and Cordero also appear to distrust the quantitative predictions of theory, citing, for example, conflicting conclusions about the feasibility of early handicap models. Although these conflicts were real, they did not result from an inherent lack of precision, but from differing underlying assumptions. We see little problem here. However, we do see persistent problems arising from errors in the interpretation and application of theory. For example, in spite of 20 years of contrary research, Co´rdoba-Aguilar and Contreras-Gardun˜o assert that genetic correlations between female preference and preferred traits are only expected under ‘traditional female choice’. This statement is false, a fact that is well known [2]. Such correlations result from assortative mating between males and females bearing alleles for the trait and preference. A hunt for such correlations, although destined for success, would be uninformative in
