To provide an inclusive estimate of the total fitness consequences of mating with an attractive or unattractive male, we quantified both the direct costs to females and the indirect benefits to their offspring. We made two main findings. First, the mating-associated costs borne by females are greater when mating to attractive males throughout their life than when they are mated to unattractive males. Second, these costs are cancelled out (when we use the rate-insensitive measure of the number of grandchildren) and may be outweighed by (when we use the rate-sensitive estimate of the intrinsic rate of increase) the benefits of having offspring with elevated fitness (i.e., indirect benefits).
Contrary to some theoretical predictions [2
], but see [1
], our results suggest that it may be possible for female mate choice to evolve via indirect benefits, despite the presence of direct costs. Whether this is the case or not will, however, depend on the magnitude of other costs of choice not measured here, such as the costs associated with being choosy, as well as the accuracy of female choice [3
The costs of choice, including the costs of mating with attractive males, are of central importance to theoretic models of mate-choice evolution [1
]. In many species females incur survival or fecundity costs due to being courted or harassed by males [30
], mating [32
], and allocating resources to egg laying, gestation, and/or parental care [34
]. Female Drosophila melanogaster
mated to large (and thus presumably attractive) males incur a greater survival cost than females mated to smaller males [21
], and this appears to be due to a higher mating rate with large males [22
]. A potential criticism of such studies is that they are based on single traits that are taken to be an indirect measure of a male's attractiveness. By using a direct biological measure that incorporates all traits that contribute to a male's ability to induce a female to mate during short-range courtship, our results provide the first direct evidence that females sustain greater direct costs when mating with males that are more attractive in this context.
While we do not know the exact mechanisms driving the survival cost seen in our experiment, our finding that females mated to more attractive males experience lower survival is consistent with sexual conflict between males and females over mating decisions [25
], and with differential allocation [34
]. Females mated to attractive males exerted greater reproductive effort in the first week of the experiment. This could be the result of male manipulation, for example, increased mating rate [32
], or stimulants in seminal fluids [36
] whereby more attractive males manipulate females to invest more in their offspring than is optimal for the females. The possibility of male manipulation is also supported by a study by Murtaugh and Denlinger [39
], which shows that in A. domesticus
, males pass substances in their ejaculate that promote higher rates of short-term oviposition. Alternatively, it may be adaptive for females to invest more in the offspring of attractive males [34
]. Differential allocation is only likely to be adaptive if there is an indirect fitness benefit to allocating greater reproductive effort when mated to attractive males [34
]. The indirect fitness benefits that we report here, particularly the benefit of having more attractive sons, may provide an adaptive basis for differential allocation by females to the offspring of more attractive males.
Several studies have reported fitness benefits of mating with attractive males. Females mated to such males have been reported to have offspring that have greater longevity [15
], faster growth rate [16
], increased fecundity of daughters [16
], and increased attractiveness of sons [19
]. In our study, the net fitness benefit of mating with attractive males is not due to any single indirect benefit but to a combination of fitness components. This illustrates the importance of measuring net fitness, especially if fitness components act in opposition to each other.
A number of studies have proposed the use of an aggregate measure of male attractiveness rather than a single morphological indicator [44
]. Our use of time to mounting allows us to gain a measure of male attractiveness that is based on all traits that contribute to male mating success (hence ‘attractiveness') during short-range courtship interactions [46
]. It is the use of such a measure that may explain the high correlation between fathers' and sons' attractiveness in this experiment and others based on similar measures [12
]. The greater attractiveness of sons sired by attractive males may also be explained by differential allocation; studies have shown that maternal effects may enhance the heritability of male traits [47
]. An important role for maternal effects is unlikely in our experiment, however, because no other fitness components of sons or daughters differ significantly between the treatments. Regardless of whether sons' greater attractiveness is due to additive genetic variation for attractiveness per se or to the ability to manipulate females into allocating more resources to the offspring, such a trait will increase a female's net fitness if it increases the reproductive success of her sons sufficiently.
Due to the nature of our experimental design we were unable to measure all the costs and benefits associated with choosing and mating with attractive males. First, we did not measure sons' ability to compete with other males for access to females. However, in this population of A. domesticus
, fighting ability has been shown to be positively correlated with attractiveness as we have measured it here [48
]. Thus, if anything we may have underestimated the fitness benefit gained through having attractive sons. Second, we did not measure long-range attraction of males through advertisement calling. Third, our design simplifies the way mating takes place for females paired with attractive or unattractive males. Pairing females with a single male for 7 d at a time may decrease or increase the costs associated with mating with males. For instance, costs may be increased because females are unable to escape male harassment, or they may be decreased because there is no male–male competition. Despite these limitations, we believe that our estimate of the intrinsic rate of increase offers a reasonable approximation of net fitness.
The fitness estimate of choice in empirical studies may depend on the importance of reproductive timing in the system in question [28
]. Brommer et al. [27
] compared estimates of lifetime reproductive success and intrinsic rate of increase to real long-term data from two species of bird. They showed that lifetime reproductive success was a better estimate of genetic contribution to future generations. However, their estimates did not include measures of offspring quality, and as they point out, their results may depend on the species life history, and the generality of their conclusions thus remains to be tested.
There are several reasons why reproducing early and having short maturation times is likely to be advantageous in crickets. First, extrinsic mortality of crickets in the wild is likely to be high. Second, females become less choosy [50
], lose condition, and produce fewer eggs as they age (M. L. Head, unpublished data). Also, individuals with shorter generation times will contribute their genes to future generations more rapidly [51
Our research constitutes one of the first attempts to directly and simultaneously test the combined direct and indirect effects of mating with males that differ in attractiveness. Only by following the effects of mating with attractive or unattractive males through at least two generations, and through both sons and daughters, is it possible to observe the combined direct effects on female lifetime fecundity and the genetic effects on offspring fitness [11
]. Although the need to conduct such a study under laboratory conditions may constrain our ability to definitively answer this question, our results suggest that indirect genetic benefits have the potential to outweigh direct costs of mating with attractive males. Moreover, this effect comes about largely, but not exclusively, due to the production of more attractive sons.