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Parasites and Sexual Selection: a Macroevolutionary Perspective University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Harold W. Manter Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of 9-1991 Parasites and Sexual Selection: A Macroevolutionary Perspective Deborah A. McLennan University of Toronto Daniel R. Brooks University of Toronto, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/parasitologyfacpubs Part of the Parasitology Commons McLennan, Deborah A. and Brooks, Daniel R., "Parasites and Sexual Selection: A Macroevolutionary Perspective" (1991). Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 250. https://digitalcommons.unl.edu/parasitologyfacpubs/250 This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. VOLUME 66, No.3 SEPTEMBER 1991 THE QUARTERLY REVIEW of BIOLOGY PARASITES AND SEXUAL SELECTION: A MACROEVOLUTIONARY PERSPECTIVE DEBORAH A. McLENNAN AND DANIEL R. BROOKS Department ofZoology, University of Toronto Toronto, Ontario, Canada M5S lAl ABSTRACT The Hamilton-Zuk hypothesis postulates a causal link between parasitism and theevolution of epigamic traits by intersexual selection. Oversimplified assumptions aboutbasic parasite biology, ambiguous formulation of thehypothesis, andpoorcommunication between ethologists andparasi­ tologists havehampered its testing. The hypothesis is supported at themicroevolutionary level iffe­ males showsignificantpreferencefor lightlyoruninfected males, if intensityof infection reflects host resistance toparasites thatdepress hostfitnessbycausingdisease, andif intensity ofinfectionisrelated tothedegree ofepigamic development. It must beshownthatparticularparasites cause disease, that thehostpopulation is polymorphic for resistance to infection by those species, and thatfemale hosts are capable ofdistinguishing malehosts with lowparasite loads duetoheritable aspects ofhostresis­ tancefrom males thatare uninfected duetochance. The macroevolutionary prediction ofthehypothe­ sis, thatspecies displaying strongly developed epigamic characters shouldhost"more parasites" than species with weaklydeveloped epigamic traits, contradicts themicroevolutionary dynamic of thehy­ pothesis, and is too ambiguous. * propose a macroevolutionary prediction based on understanding theevolutionary origin of epigamic traitsand theevolutionary origin of each host-parasite associa­ tion. Associations originating in the ancestor in which theepigamic traitappeared corroborate the hypothesis moststrongly; those originating prior to the evolution ofthe epigamic trait corroborate it weakly; those beginning aftertheoriginof theepigamic traitcouldnot havebeen involved in the originand spread of the epigamic trait. INTRODUCTION cited in Ruse, 1979: 209). Since that initial dis­ pute, numerous researchers have demonstrated HE INFLUENCE offemale choice on the that intersexual selection is an important com­ Tevolution of male epigamic characters has ponent in the mating system of a variety ofspe­ been a controversial issue since Darwin first cies (see references in Bradbury and Anders­ proposed his theory of intersexual selection son, 1987). After establishing the existence of (Darwin, 1871). Indeed, in a letter to Wallace, such a mechanism, these researchers then who had argued against the existence of female turned their attention to the question of how choice, Darwin concluded"we shall never con­ that mechanism operated. Fisher (1930) pro­ vince each other" (Darwin and Seward, 1903; posed that the development of the male charac- The Quarterly Review of Biology, September 1991, Vol. 66, No.3 Copyright © 1991 by The University of Chicago. All rights reserved. 0033-5770/91/6603-0001$01.00 255 256 THE QUARTERLY REVIEW OF BIOLOGY VOLUME 66 ter and female preference for the character fense and characters involved in host defense, would "advance together" with ever increasing produces cycles of coadaptation. This tem­ speed until the process was checked by "severe porally varying selection pressure maintains counterselection" against males bearing the a significant level of additive genetic variabil­ exaggerated trait. At the very heart of the ity for viability in the host population (Hamil­ Fisherian hypothesis lies the assumption that ton, 1982; Eshel and Aiken, 1983; Eshel and the relationship between female choice and the Hamilton, 1984; Anderson and May, 1985). preferred male character is arbitrary in terms Second, parasites adversely affect the health ofmale viability. That is, females who choose (viability) oftheir hosts. Third, the condition males with bigger tails, brighter colors, or more of male epigamic characters is an accurate and vigorous displays get nothing out ofthe inter­ direct reflection of the bearer's health (a "re­ action other than the production of male off­ vealing handicap;' Maynard Smith, 1985). spring with the preferred character (see, e.g., Consequently, the interaction between the os­ O'Donald, 1962, 1967; Lande 1981; Kirk­ cillating force of natural selection on host via­ patrick, 1982, 1986). The generality of the bility and female choice for a male character Fisherian process was challenged by propo­ that accurately communicates underlying via­ nents ofthe "good genes" school (e.g., Trivers, bility results in a form of directional intersex­ 1972; Zahavi, 1975, 1977; Borgia, 1979; An­ ual selection that does not exhaust genetic vari­ dersson, 1982, 1986; Nur and Hasson, 1983; ability in the population (see also Tomlinson, Kodric-Brown and Brown, 1984) who argued 1988). that there is an association between expression Kirkpatrick (1986) investigated the theoret­ of the epigamic character and male viability. ical implications of the Hamilton-Zukhypoth­ Because of this association, females who choose esis by performing a series of444 simulations mates with bigger tails, brighter colors, or more based on 29 sets of parameter values, includ­ vigorous displays also get mates with "better ing viabilities of genotypes, selection coeffi­ genes;' and thus produce offspring who pos­ cients, and recombination rates. He concluded sess the preferred character and are more vig­ that the mechanism, on its own, was not suffi­ orous than offspring of nonpreferred males. cient to guarantee the spread of alleles for the Unlike the Fisherian mechanism, then, the male character and female preference, partic­ "good genes" hypothesis unites superiority in ularly when both are rare in the population. attracting mates and superiority in survival He noted, however, that once these alleles, in­ ability into a mutually reinforcing force of in­ fluenced by other evolutionary forces such as tersexual selection. drift or selection on the pleiotropic effects of The chief objection to the good-genes hy­ preference, had reached some threshold fre­ pothesis comes from population genetics. Iffe­ quency, then the effects of the Hamilton-Zuk male choice of genetically "superior" males is mechanism could cause both the preference a strong enough directional force to influence and the male character to spread in a popula­ the evolutionary elaboration of the character tion. In other words, the interaction between advertising this superiority, how could genetic hosts, parasites and the origin offemale prefer­ variability, the materials of selection, be main­ ence will not initiate the process of intersexual tained in the population (Maynard Smith, selection, but may reinforce that process once 1978; Borgia, 1979; Taylor and Williams, 1982; it has begun. Pomiankowski (1987a,b) reexam­ Kirkpatrick, 1986)? Hamilton (1982)and Ham­ ined the problem by incorporating more com­ ilton and Zuk (1982) attempted to answer this plex viability assumptions into his model. objection by exploring the relationship among U sing this new set of parameters, he was able parasite fitness, host fitness, and the degree of to demonstrate that an exaggeration of the male host sexual dimorphism (see also Freeland, character and the female mating preference 1976; Zuk, 1984). Their proposal, based upon could occur if the development of the epigamic studies of parasite population structure, rests trait was a direct revealer of viability. Although upon three assumptions. First, parasites and he disagreed with Kirkpatrick about the gen­ their hosts are involved in a microevolution­ eral importance of the Hamilton and Zuk ary arms race. That is, the time lag between mechanism, he also concluded that "The'hand­ changes in characters involved in parasite of- icap principle' by itselfcannot initiate increases SEPTEMBER 1991 PARASITES AND SEXUAL SELECTION 257 in female preference when the handicap is rare. hosts and parasites, and the details of sexual It only works when a threshold value of fe­ selection (see also Endler and Lyles, 1989). male preference is exceeded, and Fisher's feed­ Although researchers disagree about the back process operates.... Both Zahavi's hand­ generality of this mechanism, they are united icap and the revealing handicap act as one-way in their proclaimed interest in the "phylogenetic directional forces which, in concert with Fisher's effects" revealed by Read (1987), Read and Har­ feedback process, lead to the runaway exagger­ vey (1989a,b), and Read and Weary (1990)
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