What role does condition dependence play in sexual selection?

Sexual selection is the dominant theory for the evolution of certain traits in animals. In 1871, Charles Darwin proclaimed that sexual selection was qualitatively different from the process of natural selection and likened this process of sexual trait evolution to artificial selection in domesticated animals. Observations have shown that in several animal species, males contain conspicuous traits, or ornaments, which appear to be redundant to the functioning and survival, despite the favorability of their female counterparts in selecting individuals with these particular traits. (Kotiaho et al 2002) Darwin offered that these traits are maintained in a species through a process of sexual selection, as opposed to natural selection, as expressing them does not enhance the individual’s rate of survival in any way. (Darwin 1871) This suggests that the secondary sex traits expressed by males must be indicative of attributes which will be advantageous to the female if she mates with the male displaying the ornament. These attributes could be a superior immune system for example, or a favourable genetic make-up. There is much evidence however, to show that expression of the ornaments or weapons displayed to attract prospective mates is costly for the bearer and from empirical observations have come models of sexual selection which predict that sexual traits are expressed in proportion to the condition of their bearer. (Andersson 1986; Darwin 1871; Kotiaho et al 2002) The role of condition dependence in sexual selection is discussed herein and we give some consideration to the reliability of experimental evidence leading to the theory of condition dependence in this instance.
Traditionally, two mechanisms are involved in the sexual selection process. The first mechanism is that of intrasexual selection involving competition between mates of the chosen sex, usually males, for access to females. Competition over mates has resulted in the evolution of weaponry traits such as horns and antlers to increase the success of mates in competitions for females. Large male size has also evolved to provide some individuals with a size advantage over others. (Andersson 1986; Duckworth 2004) The second mechanism of sexual selection involves intersexual selection, or mate choice by the choosy sex (usually females). Mate choice has resulted in the evolution of many secondary sexual traits such as the long and elaborate tail of the peacock, highly specialized courtship displays and calling songs. (Lorch et al 2003; Kotiaho et al 2002)
Competition between mates and mate choice are two mechanisms which are closely interrelated and it is likely that they both contribute to evolution through sexual selection in most species. (Kotiaho et al 2002; Møller et al 2002) Experiments demonstrate that male traits which appear to be used as weaponry in male contest competitions, such as antlers in deer, are actually the targets of female choice over mates. (Andersson 1986) It has also been suggested that contests between males make the differences between males more obvious to the choosers, thus revealing the stronger and weaker individual to enable a successful choice of mate to be made. (Candolin 1999, 2000).
In the theory of sexual selection it is an important assumption that the evolution of sexually selected traits is condition dependent. (Andersson 1986; Zeh et al 1988). According to the Handicap theory (Zahavi 1975), honest signals are costly to express and maintain and so only individuals in good enough condition can afford to invest in such extravagant mating displays. The acoustic calling song of the male cricket is a good example of a sexually selected trait which is costly to the bearer. The calling song used to attract females costs males dearly in energy expenditure, reduction in foraging time and in the increase in the risk of predation whilst performing the call. (Zuk et al 1998; Hunt et al 2001) According to Wagner and Hoback (1999), males can either increase their calling rate, produce more costly song characteristics, or both, to enhance their attractiveness to females. It is thought that the acoustic song may maintain appropriate spatial distance between neighboring males as well as being used to attract females (Wagner et al 1999). (Holzer et al 2003)
Theoretical studies suggest that the investment in ornamental traits can prevent males from being able to invest in other areas of reproduction, such as parental care, which can lead to a tradeoff between the expression of the sexual traits and care for offspring. (Candolin 1999; Kotiaho et al 2002; Andersson 1986). Such tradeoffs may result in the favour of different male mating tools which involve the investment in the traits which give them maximum fitness. (Holzer et al 2003) It is believed that alternative reproductive investments such as these coexist in a single animal population because there is variation in the availability and utilization of resources among males and these may favor the variety of male who solves a reproductive trade-off in a particular way. In some species practising biparental care, for example, (such as the dung beetle Onthophagus Taurus (Hunt et al 2001)) males express either competitive or parental behaviour depending on whether the investment is in the parental or competitive trait (Holzer et al 2002)
Current models of sexual selection predict that, because sexual traits are costly, they should positively co-vary with the condition of the possessor. (Andersson 1986). That is, the cost of expressing a secondary sexually selected ornamental trait is effectively negated by a high level of fitness. Empirical studies reveal that the expression of a secondary sexually selected trait is influenced by environmental factors such as resource availability, predation and parasitism risk, as well as by genetics. (Zuk et al 1993) Furthermore, as long as condition dependent traits are indicative of the phenotypic or genotypic quality of the male, it is beneficial to the females to include condition dependence in mate choice decisions. (Holzer et al 2002; Andersson 1986) Being able to predict the condition dependence of sexual traits is thus particularly important for the identification of indicators of viability as condition dependence itself acts as a condition to indicate quality (Andersson, 1986; Zahavi, 1975) Expression of condition dependence in sexual traits plays an important role in the theory of good genes sexual selection. (Byers et al 2006; Andersson 1986) Due to the fact that we do not expect there to be much genetic variation in traits closely related to fitness (Byers et al 2006), we are persuaded that there is not much in the way of prospects for female choice to result in genetic advantage. If we assume that there is genetic variance in condition itself and sexual traits exhibit good condition dependence, we can negate this ‘lek paradox’. For this reason, condition-dependent expression of sexual traits has an important role in the theory of sexual selection. (Tomkins2004)
The empirical evidence suggesting that sexually selected traits and displays are condition dependent is accumulating and it is becoming widely accepted that that most traits show some degree of condition dependence. However, like most processes in nature, condition dependent expression of traits is not always straight forward. For example, in the three-spined stickleback, the red colour of the males which is important in the process of mate selection is positively condition dependent. However, experiments have demonstrated that whilst the red colouration is indicative of fit males, it is also expressed in poorly conditioned males. (Bakker et al 1999;Candolin, 1999, 2000).
More experimental investigation into condition dependence is required if we are to better understand the relationship between the expression of sexual traits and condition dependence. (Bakker et al 1999; Candolin 1999, 2000; Holzer et al 2003; Andersson 1986; Møller et al 2003) Most studies which have investigated the condition dependence of certain sexually selected traits and their effect on female mate choice have been performed under experimental conditions and not in nature and the reliability of the results is thus questionable. (Andersson 1986). In addition, the studies cannot divulge information on how males make optimal use of resources whilst exhibiting the sexually selected trait in a natural habitat. Variation in resource availability, temperature, intraspecific competition, as well as risk of predation and parasitism may influence the trade-off outcome between investment in the trait and other life history traits, as mentioned above. (Anderson 1986; Holzer et al 2003)
Scrutiny of the term condition and what constitutes it is hugely important when considering condition dependence in sexual selection as quantification of condition is very difficult. Kotiaho (1999) terms the phenomenon ‘abstract’ and claims that it is near impossible to ‘really know what constitutes a good empirical measure of condition’. (Kotiaho 1999). In terms of sexual selection models, it is agreed by some that condition must be seen as the individual’s ability to reflect the overall source of resources which are available for the investment in different traits. Thus a high degree of fitness is attributable to condition. (Cotton et al 2007) The failure to agree on a quantitative measure of condition has remained a limiting factor in the ability to make predictions about sexually selected traits and will continue to do so.