Advantages of Multiple Mating in Female Guppies

The evolutionary party line has traditionally been that males increase reproductive success by mating with multiple females, but females enjoy no such advantage or, more modestly, the advantage isn’t as great. This line has been drawn in no small part on Bateman’s early work on fruit flies. The work, and the broader idea, has recently been the subject of no small amount of discussion and debate.

So… you got any friends, big boy…?

A new paper now available online from BMC Evolutionary Biology by Miguel Barbosa and colleagues entitled “Fitness consequences of female multiple mating: A direct test of indirect benefits” addresses the question of what advantages, if any, accrue to females by mating with multiple males. In this case, the subject of their investigation was Poecilia reticulata, the Trinidadian guppy.

The terms “direct benefits” and “indirect benefits” the authors use in the title of the paper refer to two sorts of ways that a female guppy might improve her reproductive success by mating with more than one male. (Roughly this corresponds to quantity/quality of offspring. I confess I’m not thrilled with these terms here, but I’ll stick with the authors’ choices.) One type of direct benefit – having more offspring per se –could be from the increased possibility of a female having all her eggs fertilized, should the sperm from one male be insufficient. In such a case, the advantages should be apparent and measurable in the number of offspring produced (the so-called F1 generation). Indirect benefits, in contrast, come from producing offspring that have some (genetic) advantage in the F1 generation itself. That is, females don’t have more offspring, but the offspring that they do have enjoy higher fitness. For instance, suppose that multiple matings allows a female’s eggs to be fertilized by sperm that do well in competition with other sperm in the reproductive tract. Males in the F1 generation would then be more likely to have this trait, conferring an advantage, which might then be visible by comparing males from females who mated multiply with females who mated singly. This requires looking at the F2 generation.

This is exactly what Barbosa et al did. Female guppies were given their own tank, and divided into two groups. Guppies in the single mating group were allowed to mate with a male on day 1, and then allowed to mate with that same male again over the course of the next three days. Guppies in the multiple mating group similarly had access to one male for four days, but it was a different male each day. Offspring from the matings of both groups were themselves allowed to mate, producing the F2 generation.

They found that multiply mated females did enjoy greater reproductive success, as measured by the number of grand-offspring produced. Indeed, this advantage was large, greater than a factor of two. Where did the advantage come from? It was driven by advantages in the F1 generation. The authors find:

Multiply mated females produced 60% more viable F1 offspring, on average, than singly mated females…In the next generation, there were no significant differences in the reproductive success of individual F1 that had been produced from multiple versus single matings

Caption from the paper: Direct Fitness (F0 to F1). Mean number of viable offspring (F1) produced by singly or multiply mated F0 females, counting (A) all F1, (B) male F1, and (C) female F1.

So, singly mated females produced significantly fewer offspring than multiply mated females. As you can see in Figure 2, this difference between the two groups was due to the significantly greater number of male F1 offspring.

In the authors’ own words, from their findings they conclude:

Our results strongly support the hypothesis that multiple mating is adaptive, as manifested by an increase in female fecundity. We found that multiply mated females produce substantially more grand-offspring than singly mated females. However, because the reproductive output (F2) of progeny from multiply and singly mated females was not significantly different, we also showed that this fitness advantage is driven by the production of more offspring in the first generation (F1), rather than by elevating the fitness of offspring (second-generation effects).

They do not rule out the possibility that there are also indirect (genetic) benefits of multiple matings. The experimental procedures might have masked such benefits that might have been found in more natural populations.

In any case, this adds to the growing body of evidence that females benefit from mating with multiple males. To the extent that females do gain such benefits, the party line difference of a greater male advantage to multiple mating and female advantage to multiple mating, across taxa, seems to be getting even fuzzier.

Reference

Barbosa, M., Connolly, S. R., Hisano, M., Dornelas, M., & Magurran, A. E. (2012).  Fitness consequences of female multiple mating: A direct test of indirect benefits. BMC Evolutionary Biology, 12(185). doi:10.1186/1471-2148-12-185

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