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Sex-Ratio Control Erodes Sexual Selection, Revealing Evolutionary Feedback from Adaptive Plasticity

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Sex-Ratio Control Erodes Sexual Selection, Revealing Evolutionary Feedback from Adaptive Plasticity Sex-ratio control erodes sexual selection, revealing evolutionary feedback from adaptive plasticity Tim W. Fawcett1,2,3, Bram Kuijper1,4, Franz J. Weissing, and Ido Pen Theoretical Biology Group, University of Groningen, 9700 CC, Groningen, The Netherlands Edited by Stuart West, Oxford University, Oxford, United Kingdom, and accepted by the Editorial Board August 1, 2011 (received for review April 11, 2011) Female choice is a powerful selective force, driving the elaboration principle extends to a wide range of other contexts in which se- of conspicuous male ornaments. This process of sexual selection lection favors phenotypic plasticity in response to a directionally has profound implications for many life-history decisions, includ- selected trait. ing sex allocation. For example, females with attractive partners should produce more sons, because these sons will inherit their Model father’s attractiveness and enjoy high mating success, thereby Basic Scenario. For the sake of tractability, we consider just two yielding greater fitness returns than daughters. However, previ- types of males, which differ in their ornamentation (5, 11, 12): ous research has overlooked the fact that there is a reciprocal those of type 0 lack ornamentation, whereas those of type 1 are feedback from life-history strategies to sexual selection. Here, using ornamented to a degree given by the evolvable trait t (t $ 0). a simple mathematical model, we show that if mothers adaptively Ornamentation is costly in that it reduces survival to adulthood, control offspring sex in relation to their partner’s attractiveness, with the relative survival of type-1 (compared with type-0) males sexual selection is weakened and male ornamentation declines. This given by vm1 (vm1 # 1). This cost reflects the energy or resources weakening occurs because the ability to determine offspring sex invested in the development of secondary sexual traits or an reduces the fitness difference between females with attractive associated predation risk of being conspicuous (1). and unattractive partners. We use individual-based, evolutionary Females are of one type only and have an evolvable preference simulations to show that this result holds under more biologically p (p $ 0), which is costly and lowers their survival to vf (vf # 1). realistic conditions. Sexual selection and sex allocation thus interact This cost may arise because the female has to invest in sensory EVOLUTION in a dynamic fashion: The evolution of conspicuous male ornaments apparatus for assessing males, or because she incurs a higher favors sex-ratio adjustment, but this conditional strategy then predation risk while choosing a mate (13). Her preference makes undermines the very same process that generated it, eroding sexual her more inclined to mate with an ornamented than a non- selection. We predict that, all else being equal, the most elaborate ornamented male, resulting in a proportion α of females that sexual displays should be seen in species with little or no control mate with the former type (note that α is not fixed but depends over offspring sex. The feedback process we have described points on p, t, and the relative frequencies of type-0 and type-1 males). to a more general evolutionary principle, in which a conditional Consequently, the expected number of mates is q1 for an orna- strategy weakens directional selection on another trait by reducing mented male and q0 for a nonornamented male, with q1 $ q0. fitness differences. Crucially, females can adjust offspring sex ratios in relation to their partner’s ornamentation: Sex allocation is determined by evolutionary equilibrium | Fisher process | good genes | phenotypic the evolvable traits s0 and s1, where s0 is the proportion of sons plasticity | sex-ratio bias produced when mated to a nonornamented male and s1 the proportion when mated to an ornamented male. Ornamentation onspicuous male ornaments such as brightly colored or is heritable from father to son, except when mutations occur: μ elongated feathers, loud vocalizations, and complex court- With probability 0, the son of a nonornamented male is orna- C μ ship dances are the hallmark of sexual selection, maintained mented, and with probability 1, the son of an ornamented male despite their obvious costs because females find them attractive is nonornamented. In common with standard models of sexual (1). This evolutionary force has profound implications for many selection (14, 15), we assume that mutations are biased toward μ > μ life-history decisions, including which sex of offspring to produce the loss of ornamentation, i.e., that 1 0. This bias prevents fi fi and how to invest in them (2–4). Provided the heritable benefits xation of the male ornament and thereby preserves the bene t of ornamentation are to some degree sex-limited, selection of female choice (15). Individuals are assumed to die before their favors a conditional strategy of sex allocation: Females mated to offspring become reproductively mature, so that generations are attractive, highly ornamented males should overproduce sons, nonoverlapping. Fig. 1 summarizes the sequence of events in our whereas those mated to unattractive males should overproduce model. Table 1 lists the variables and parameters with their daughters (3). This pattern of sex allocation has been supported associated symbols. by a number of theoretical (5–7) and empirical (8–10) studies, but no one has considered how it might feed back to alter sexual selection. Here, we investigate the dynamic interplay Author contributions: T.W.F., B.K., F.J.W., and I.P. designed research; T.W.F., B.K., and I.P. fi performed research; T.W.F., B.K., and I.P. analyzed data; and T.W.F., B.K., F.J.W., and I.P. between sexual selection and sex-ratio adjustment. We rst de- wrote the paper. velop a simple mathematical model in which male ornamenta- The authors declare no conflict of interest. tion, female preference, and the sex-allocation strategy can This article is a PNAS Direct Submission. S.W. is a guest editor invited by the Editorial coevolve and use this model to determine the direction of se- Board. lection acting on all of these traits. We then extend our analysis 1T.W.F. and B.K. contributed equally to this work. to more biologically realistic conditions by using a series of 2To whom correspondence should be addressed. E-mail: [email protected]. individual-based, evolutionary simulations, incorporating con- 3 fi Present address: School of Biological Sciences, University of Bristol, Bristol BS8 1UG, tinuous variation in ornamentation and preference, a nite United Kingdom. population size, and stochastic factors such as genetic drift. This 4Present address: Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, dual approach allows us to uncover the evolutionary forces United Kingdom. linking sexual selection and sex allocation. After analyzing this This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. coevolutionary feedback process in depth, we show how the same 1073/pnas.1105721108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1105721108 PNAS Early Edition | 1of6 Downloaded by guest on September 28, 2021 approach involves three basic steps: (i) Determine the dynamics of a resident population with trait value x for a given trait of interest; (ii) determine the invasion fitness of a rare mutant with alternative trait value ^x within this resident population; and (iii) determine how mutant fitness w depends on x and ^x. Below we outline these steps in detail. Dynamics of the Resident Population. We first consider the dy- namics of a resident population with ornamentation level t, preference p, and sex-allocation traits s0 and s1. The numbers of females, type-0 males, and type-1 males change from one gen- eration to the next according to the transition matrix 2 3 ½ð1 − αÞð1 − s0Þþαð1 − s1Þvf q0ð1 − s0Þvf q1ð1 − s1Þvf A ¼ 1 k4 ½ð − αÞs ð − μ Þþαs μ v q s ð − μ Þv q s μ v 5: 1 0 1 0 1 1 m0 0 0 1 0 m0 1 1 1 m0 2 ½ð − αÞs μ þ αs ð − μ Þv q s μ v q s ð − μ Þv 1 0 0 1 1 1 m1 0 0 0 m1 1 1 1 1 m1 [1] The factor 1/2 is a formality to prevent offspring being counted twice (once via its mother and once via its father), whereas the constant k is a scaling factor (equivalent to the average clutch size) to ensure that the population is stable (in technical terms, to ensure that the dominant eigenvalue is 1; see refs. 18 and 19). The leftmost column of A represents the per-capita reproductive output of females, the center column that of type-0 males, and the rightmost column that of type-1 males. The three rows rep- resent, from top to bottom, the result of this reproductive output in terms of surviving females, type-0 males, and type-1 males in the next generation. The entries in the matrix are derived from the basic assump- tions of our model. To give an example, take the leftmost entry in the center row, which represents the reproductive contribution of mothers to type-0 males in the next adult generation. There are two scenarios in which a female gives birth to a type-0 son: either she mates with a type-0 male (probability 1 − α) and Fig. 1. Summary of the sequence of events in each generation of our produces a son (probability s0) who is unaffected by mutation model. The survival of females (vf) and ornamented males (vm1)tore- (probability 1 − μ0), or she mates with a type-1 male (probability production is reduced by the cost of their preference and ornament, re- α s spectively (nonornamented males do not pay a cost; vm0 = 1).
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