Andrew Pomiankowski

Why have birds got multiple sexual ornaments

SummaryMales of many animals have more than a single exaggerated secondary sexual character, but inter-specific variability in the number of ornaments has never been explained. We examine three hypotheses that may account for the presence of multiple ornaments. First, the multiple message hypothesis proposes that each display reflects a single property of the overall quality of an animal. This is likely to be the case for ornaments that respond to condition on different time scales. Second, the redundant signal hypothesis suggests that each ornament gives a partial indication of condition. Females pay attention to several sex traits because in combination they provide a better estimate of general condition than does any single ornament. The redundant signal hypothesis predicts that (i) multiple ornaments should be particularly common among taxa with relatively uncostly and fine-tuned female choice, and (ii) females pay equal attention to the expression of all the secondary sex traits in order to obtain an estimate of overall male condition. Finally, the unreliable signal hypothesis argues that some ornaments are unreliable indicators of overall condition and are only maintained because they are relatively uncostly to produce and there is a weak female preference for them. This predicts that (i) multiple sexual ornaments should be particularly common in taxa with the most intense sexual selection (i.e. lekking and other polygynous taxa), and (ii) there should be more evidence for condition dependence in ornaments of species with single as opposed to multiple ornaments. Both the latter predictions are supported by data on feather ornaments in birds.

A Resolution of the Lek Paradox

Sexual traits are usually more phenotypically variable than non-sexual traits. We show that additive genetic variation is also higher in sexual traits, and often greater than in the same, non-sexually selected trait in females or other comparable traits in the same species. In contrast there is no difference in residual variation (environmental and non-additive) or heritability. The higher genetic variability of sexual traits is contrary to the expectations of the lek paradox. This hypothesis predicts that strong sexual selection, due to female choice, leads to fixation of most genetic variation in male sexual characters. High genetic variability in sexual traits can be explained if they are subject to directional selection that is greater than linear because this selects for greater phenotypic variation. It favours modifiers that increase the number of genes and the average contribution of a locus to phenotypic variance in sexual traits. These results provide a general resolution of the lek paradox.

Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis?

The handicap hypothesis of sexual selection predicts that sexual ornaments have evolved heightened condition–dependent expression. The prediction has only recently been subject to experimental investigation. Many of the experiments are of limited value as they: (i) fail to compare condition dependence in sexual ornaments with suitable non–sexual trait controls; (ii) do not adequately account for body size variation; and (iii) typically consider no stress and extreme stress manipulations rather than a range of stresses similar to those experienced in nature. There is also a dearth of experimental studies investigating the genetic basis of condition dependence. Despite the common claim that sexual ornaments are condition–dependent, the unexpected conclusion from our literature review is that there is little support from well–designed experiments.

FLUCTUATING ASYMMETRY AND SEXUAL SELECTION

Fluctuating asymmetry occurs when an individual is unable to undergo identical development on both sides of a bilaterally symmetrical trait. Fluctuating asymmetry measures the sensitivity of development to a wide array of genetic and environmental stresses. We propose that fluctuating asymmetry is used in many signalling contexts for assessment of an individuals ability to cope with its environment. We hypothesize that fluctuating asymmetry is used in sexual selection, both in fighting and mate choice, and in competition for access to resources. Evidence is reviewed showing that the patterns of fluctuating asymmetry in secondary sexual characters differ from those seen in other morphological traits. Secondary sexual characters show much higher levels of fluctuating asymmetry. Also, there is often a negative relationship between fluctuating asymmetry and the absolute size of ornaments, whereas the relationship is typically U-shaped in other morphological traits. The common negative relationship between fluctuating asymmetry and ornament size suggests that many ornaments reliably reflect individual quality.

The evolution of costly mate preferences. I, Fisher and biased mutation

Fishers runaway process is the standard explanation of the evolution of exaggerated female preferences. But mathematical formulations of Fishers process (haploid and additive diploid) show it cannot cause stable exaggeration if female preference carries a cost. At equilibrium female fitness must be maximized. Our analysis shows that evolutionary stable exaggeration of female preference can be achieved if mutation pressure on the male character is biased, that is, mutation has a directional effect. At this equilibrium female fitness is not maximized. We discuss the reasons and evidence for believing that mutation pressure is typically biased. Our analysis highlights the previously unacknowledged importance of biased mutation for sexual selection.

Sexual Selection and Condition-Dependent Mate Preferences

The last decade has witnessed considerable theoretical and empirical investigation of how male sexual ornaments evolve. This strong male-biased perspective has resulted in the relative neglect of variation in female mate preferences and its consequences for ornament evolution. As sexual selection is a co-evolutionary process between males and females, ignoring variation in females overlooks a key aspect of this process. Here, we review the empirical evidence that female mate preferences, like male ornaments, are condition dependent. We show accumulating support for the hypothesis that high quality females show the strongest mate preference. Nonetheless, this is still an infant field, and we highlight areas in need of more research, both theoretical and empirical. We also examine some of the wider implications of condition-dependent mating decisions and their effect on the strength of sexual selection.

The costs of choice in sexual selection.

In Fishers model of sexual selection female mating preferences are not subject to direct selection but evolve purely because they are genetically correlated with the favoured male trait. But when female choice is costly relative to random mating, for example in energy, time or predation risks, the evolution of female mating preference is subject also to direct selection. With costly female choice the set or line of equilibria found in models of Fishers process no longer exists. On the line the male trait is under zero net selection, and there is no advantage for a female choosing a male with a more exaggerated character. Therefore any cost to choice causes choosiness to decline. In turn this lowers the strength of sexual selection and the male trait declines as well. So when Fishers process is the sole force of sexual selection and female choice is costly, only transitory increases in female choice and the preferred male trait are possible. It has often been claimed that exaggerated male characters act as markers or revealers of the genetic quality of potential mates. If females choose their mates using traits that correlate with heritable viability differences then stable exaggeration of both female choice and the preferred male character is possible, even when female choice is costly. The offspring of choosy females have not only a Fisherian reproductive advantage but also greater viability. This suggests that in species with exaggerated male ornamentation, in which female choice is costly, it is likely that female mate choice will be for traits that correlate with male genetic quality.

Condition-dependent signalling of genetic variation in stalk-eyed flies

Handicap models of sexual selection predict that male sexual ornaments have strong condition-dependent expression and this allows females to evaluate male genetic quality. A number of previous experiments have demonstrated heightened condition-dependence of sexual ornaments in response to environmental stress. Here we show that genetic variation underlies the response to environmental stress (variable food quality) of a sexual ornament (male eye span) in the stalk-eyed fly Cyrtodiopsis dalmanni. Some male genotypes develop large eye span under all conditions, whereas other genotypes progressively reduce eye span as conditions deteriorate. Several non-sexual traits (female eye span, male and female wing length) also show genetic variation in condition-dependent expression, but their genetic response is entirely explained by scaling with body size. In contrast, the male sexual ornament still reveals genetic variation in the response to environmental stress after accounting for differences in body size. These results strongly support the hypothesis that female mate choice yields genetic benefits for offspring.

THE EVOLUTION OF MATE PREFERENCES FOR MULTIPLE SEXUAL ORNAMENTS.

Males of many species use multiple sexual ornaments in their courtship display. We investigate the evolution of female sexual preferences for more than a single male trait by the handicap process. The handicap process assumes that ornaments are indicators of male quality, and a female benefits from mate choice by her offspring inheriting “good genes” that increase survival chances. A new handicap model is developed that allows equilibria to be given in terms of selection pressures, independent of genetic parameters. Multiple sexual preferences evolve if the overall cost of choice is not greatly increased by a female using additional male traits in her assessment of potential mates. However, only a single preference is evolutionarily stable if assessment of additional male traits greatly increases the overall cost of choice (more than expected by combining the cost of each preference independently). Any single preference can evolve, the outcome being determined by initial conditions. The evolution of one preference effectively blocks the evolution of others, even for traits that are better indicators of male quality. Comparison is made with sexual selection caused by Fishers runaway process in which male traits are purely attractive characters. This shows that sexual preferences for multiple Fisher traits are likely to evolve alongside preference for a single handicap trait that indicates male quality. This is a general difference in the evolutionary outcome of these two causes of sexual selection.

SEXUAL SELECTION - THE HANDICAP PRINCIPLE DOES WORK SOMETIMES

Zahavi’s ‘handicap principle’ proposes that females prefer males with handicaps (mating characters that reduce survival chances) because handicaps are indicators of heritable viability. It is shown here that there are conditions under which the ‘handicap principle’ causes the runaway exaggeration of male handicaps and female mating preferences. The conditions required are (a) that the fitness effects of the handicap and ‘viability’ genes combine non-multiplicatively (Zahavi’s handicap), and/or (b) that the handicap should directly reveal the presence or absence of genes for high viability (the revealing handicap). The ‘handicap principle’ by itself cannot initiate increases in female preference when the handicap is rare. It only works when a threshold value of female preference is exceeded, and Fisher’s feedback process operates. When Fisher’s feedback process occurs alone, a line of equilibria exists, where for each intensity of female preference there is a corresponding equilibrium development of the male mating character. When the ‘handicap principle’ also operates, the internal line of equilibria is eliminated, and only boundary equilibria persist (i. e. fixation or loss of the handicap). All populations at what were previously internal equilibria, or in which the intensity of female preference is above threshold, increase in a runaway to fixation of the handicap; therefore, handicapping male mating characters are more likely to be exaggerated when they are also indicators of viability.