In the context of sexual selection, GxEs are likely to be very important. They could affect the expression of both male sexual traits and female mating preferences for them, which would ultimately influence how these traits co-evolve. Furthermore, GxEs might account for claims that sexual selection generates limited evolution in some free-living populations (Grant & Grant, 2002). However, this is a relatively new field of research, and even theoretical studies are yet to consider many of the possible ways in which GxEs could potentially influence the evolution of male sexual traits. So far, models have explored how GxEs could disrupt the reliability of sexual signals (Higginson & Reader, 2009) and how they might facilitate the maintenance of variation in sexually selected traits (Kokko & Heubel, 2008).
The reliability of sexual traits as signals
Many models of sexual selection and the evolution of female mating preferences require that male sexual traits reliably signal some aspect of male quality that enables females to benefit from costly mate choice (Zahavi, 1975; Grafen, 1990; Johnstone, 1995). These benefits can be either direct to the female through materials and resources that might help her produce and raise offspring, or indirect through heritable genetic gains for offspring. If only high-quality males are capable of producing exaggerated sexual signals, then females can assess male quality via the sexual trait, secure fitness benefits, and female mate preferences will be advantageous (Grafen, 1990).
However, there are a number of circumstances in which GxEs in male sexual signals could disrupt signal reliability, causing females to effectively make the ‘wrong’ mating decision (Greenfield & Rodriguez, 2004). As an example, consider male bushcrickets that call to attract females using specialized structures on the wings that are fixed at eclosion to adulthood. During mate choice, females use calls to assess male quality, choosing to mate with high-quality males that are able to produce large, nutrient-rich spermatophores. However, if the environment changes between when males develop their wings and when they become sexually mature and start calling, or similarly if migration occurs between these times, then wing morphology, and the resulting quality of song a male produces, represents his condition and quality in the initial environment which is no longer relevant. Consequently, females might choose a male based on an attractive call, but receive a poor quality spermatophore in return. In this way, GxEs in heterogeneous environments could cause the signal received by the female to be an unreliable indicator of the quality of the male and of the benefits he can provide (Higginson & Reader, 2009), and this will have implications in the evolution of mating preferences and could potentially eliminate any selective advantage to mate choice in the first place.
Equally, females can use male sexual signals to assess genetic quality. Indirect genetic benefits are generally mediated through genes that either confer sexual attractiveness or viability to offspring, and studies have found that attractive males do sire attractive sons, for example (e.g. crickets, Wedell & Tregenza, 1999; flies, Taylor et al., 2007). However, the reliability of indicators of male attractiveness could be disrupted by GxEs and environmental fluctuations in the same manner as the direct benefits discussed earlier (Kokko & Heubel, 2008; Higginson & Reader, 2009), as could the reliability of viability indicators. For instance, male sticklebacks (Gasterosteus aculeatus) in good condition can produce brightly pigmented patterns that are attractive to females. In populations with parasites, condition is correlated with resistance to infection, and so females can use these sexual signals as indicators of viability genes which confer parasite resistance to her offspring (Barber et al., 2001). However, parasite populations will vary both spatially and temporally, creating situations where a male might develop in the absence of parasites and then produce an attractive signal despite not being resistant to infection.
The issue of signal reliability is likely to be even more complex when females assess multiple sexual traits during mate choice, as appears common in many species (Candolin, 2003). For example, in the field cricket, Gryllus campestris, males produce an advertisement call to attract a mate, and females prefer males that produce calls with an increased chirp rate (Holzer et al., 2003) and a lower carrier frequency (Simmons & Ritchie, 1996). Carrier frequency and chirp rate are uncorrelated components of the call (Holzer et al., 2003; Scheuber et al., 2003a), and carrier frequency, but not chirp rate, is negatively correlated with adult body size. Carrier frequency reliably signals juvenile, but not adult, condition with juveniles experiencing good nutrition during development growing larger and producing a call with a lower carrier frequency (Scheuber et al., 2003b). Conversely, chirp rate is not influenced by juvenile condition but reliably signals adult condition, with adults fed a more nutritious diet calling at an increased chirp rate (Scheuber et al., 2003a). Consequently, if individuals occupy heterogeneous environments and there are GxEs for these traits, then the signal content of them can become uncoupled, making it difficult for a female to fulfil both preference criteria reliably. It is even possible that females will receive conflicting information from the traits they are assessing (i.e. a male producing a high carrier frequency but producing a high chirp rate).
The reliability of sexual signals is a key assumption in most models of sexual selection, because if not, selection for costly mate choice should be significantly weakened. Some models even predict that mate choice should not evolve in populations where this positive correlation does not exist (Kokko et al., 2006). Two recent models that have considered how GxEs can influence signal reliability use different modelling approaches, but largely reach the same conclusion (see Box 1). That is, interactions modelled both with and without ecological crossover can disrupt the reliability of sexual signals (Kokko & Heubel, 2008; Higginson & Reader, 2009) and, under certain conditions, can result in a negative correlation between female preference and male quality (Higginson & Reader, 2009). This situation is not predicted by classical models of sexual selection but clearly indicates how important GxEs could be in sexual selection.
Kokko & Heubel (2008) explored sexual signal reliability by modelling the costs of mating preferences tolerated by females, which is used as a proxy for the strength of female mating preferences (see Box 1). Where GxEs exist in sexual trait expression, a major cost could be the potentially low information content of male signals of quality, and the resulting increased chance that a female will make a mistake when expressing mate choice. The model looks at how gene flow between environments affects the costs of female mating preferences, and the results clearly indicate that selection for female mating preferences disappears under high levels of gene flow (with environmental structure) (see Box 1). This could be attributed to the high costs of female mate choice, which result from the low reliability of male sexual signals, which are in turn caused by GxEs and environmental variation (change).
Higginson & Reader (2009) test the potential effect of GxEs on sexual signal reliability by modelling the information content of sexual signals. Interestingly, the model highlights the importance of both genetic variation and environmental variation: signal reliability can potentially be compromised both by reduced genetic variation and by increased environmental variation (see Box 1). The model also emphasizes the influence of harsh, or stressful, environmental conditions that can severely reduce the information content of sexual signals.
The next obvious theoretical step would be to consider the consequences of unreliable sexual signals on the evolution of female mate preferences. It follows that selection for female choice will be weakened if male sexual traits do not reliably signal some female benefit. This potentially has knock-on effects for trait and preference evolution. Indeed, Greenfield & Rodriguez (2004) suggested that signal reliability in traits affected by GxEs can only be fully maintained when the reaction norms for the size of the male trait and the corresponding female preference are parallel across environments.
Alternatively, it is possible that some information is better than none at all, meaning that even when GxEs exist for male sexual traits, females that utilize the little information in these signals have less variance in fitness than females not using ‘unreliable’ signals. Again, this needs explicit testing, by, for example, comparing female choice benefits in constant environments and fluctuating environments, with females not given a choice of mates. Either way, empirical research needs to look at both male trait expression and female mating preferences to account for the coevolution of sexual traits.