That cricket song? Maybe he's just whistling Dixie after all

Science last week published a cautionary tale--"Natural and Sexual Selection in a Wild Insect Population"--about the limits of observations made in the lab, but in fact it suggests limits to what 'everyone knows', as well. The paper was accompanied by a commentary by Marlene Zuk. 

The authors, R. Rodríguez-Muñoz et al., point out that most studies of reproductive success among invertebrates are carried out in the lab, while those on vertebrates more often take place in the field. They set out to compare observations of reproductive success, and therefore determinants of fitness, among crickets in the field with conventional wisdom gained from observations in the lab.

Although poorly understood in their natural habitats, crickets have become an important laboratory model system, revealing complex forms of sexual selection whereby females choose between males according to their songs, males fight, females manipulate sperm from several males to favor unrelated males, and females lay eggs faster when mated to dominant males. However, although we now have many insights into the behavior and physiology of crickets in the laboratory, we have almost no idea how important these various aspects are in the insects’ natural habitat. This discrepancy is a cause for concern: Laboratory situations remove some sources of selection that may be very important in wild populations and may create new pressures; for instance, it may be that males that sing more get more mates in the lab, but in the field such males may die younger.

Rodríguez-Muñoz et al. set up a series of motion-activated cameras to monitor the comings and goings of these flightless burrow-dwelling field crickets (Gryllus campestris, as pictured in the drawing above), and confirmed paternity with DNA testing, in this way following 2 generations of crickets. They labeled each cricket, and noted each one's behavior, including fights between males, who won and who lost, as an indicator of dominant or subordinate behavior.

Perhaps surprisingly, they found that mating success didn't necessarily correlate with reproductive success, or number of offspring.  And they found some inconsistencies between what theory predicts and what they actually observed.

They report greater variance in reproductive success among males than among females, which is consistent with current theory, but this wasn't because males had more mates than females, as they found no difference in variance in number of mates between the sexes. Crickets of both sexes who had more lifetime mates had more offspring--this was true even for females that used only sperm from the single ejaculate of one male, even if they had multiple mates (this was confirmed by DNA testing).

Reproductive success was also correlated with size and lifespan--larger, longer-lived individuals of both sexes left more offspring. Among males, dominance and the 'interaction between size and singing activity' were predictive of mating success (smaller males who sang more had more mating opportunities), but offspring number was predicted by the interaction between size and singing (again, smaller males had more offspring when they sang more), and longevity and singing, but not by dominance. This is contrary to what has been found in the lab, where dominant males have greater numbers of offspring--and contrary to long-standing theory about the fitness effects of dominance behavior applied to vertebrates and invertebrates alike.

Long-standing theory also predicts that singing and size are sexually selected traits that demonstrate higher genetic quality, and that, therefore, larger males who sing a lot will have more offspring than their smaller quieter neighbors. However, in this population of crickets at least, these traits don't seem to be indicators of genetic condition, or if they are, they don't necessarily lead to increased fitness, or more descendants.

So, dominance, size, singing activity, number of mates, all of which are assumed to be either directly or indirectly correlated with reproductive success, are not predictive of either mating success or number of offspring in these crickets.  Indeed, and this is perhaps the most startling finding of this study (at least to those interested in documenting a genetic basis for behavior), most crickets left no offspring at all. As Zuk says,

Contrary to theory, or at least to common assumptions about animal behavior and ecology, was the discovery that the vast majority of individuals, whether male or female, did not successfully reproduce at all. Although males are often acknowledged to play a high-stakes, high-risk game with many losers, conventional wisdom has it that virtually all females, even those in relatively poor condition, should be able to eke out at least one or two young; this disparity underlies, for example, the Trivers-Willard effect on sex ratio, in which mothers in poor condition are predicted to favor daughters over sons because even low-quality females are expected to be able to reproduce. Yet none of the female G. campestris and only a couple of the males had more than 10 surviving offspring and most had none, despite the ability of females to lay scores of eggs.

Rodrîguez-Muñoz et al. conclude that most of their laboratory observations are upheld in the field. But there's a lot of "contrary to theory" in this story.  And--this is our conclusion, not theirs--it seems that Nature can fine-tune those traits that are supposed to indicate genetic quality or that attract mates as much as She wants to, but none of that will guarantee reproductive success.   No matter how fine their song or how many fights they win, most crickets don't reproduce at all.

As we have written a number of times, when it comes to evolutionary success, chance and good luck have the upper hand more often than many of us like to think. And extrapolation from current observations, lab or field, to the evolutionary scale of thousands or millions of generations, in different ecological and physical habitats, is usually too risky to justify the lack of circumspection in so many evolutionary scenarios eagerly advanced by evolutionary behaviorists.