Title: Strangers and Sex - the role of familiarity in guppy mate choice
Author: Nirvana Naidoo
Category: UNSW Research


Over the summer, I participated in the UNSW Faculty of Science Undergraduate Vacation Research Scholarship program, open to science students in second year and above. I completed a research project on sexual selection in guppies with Dr Rob Brooks of the School of Biological, Earth and Environmental Sciences, gaining valuable practical experience as well as insight into what is involved in scientific research.

Survival of the fittest often summons images of the strongest or fastest. Yet even such an individual is evolutionarily insignificant if he or she fails to pass on any of his or her genes. Natural selection occurs because there is genetic variation between individuals causing some, for example, to live longer or be better at gathering food. The fittest individuals leave the most descendants, and to do that they must be better than their competitors at finding resources and escaping predators. In many species, however, we find traits that do not increase an individual’s chance of surviving to reproduce but may in fact hinder it. Traitsm such as the brightly coloured and ornate tails of some male birds and fish, make them easier targets for predators. Yet these traits persist.

The theory of natural selection cannot explain the existence of seemingly exaggerated traits, such as the peacock’s tail, leading Darwin to the idea of sexual selection, a special case of natural selection. Under sexual selection, phenotypic variation in a trait in one of the sexes, usually male, results in differential mating success. Sexual selection can occur either by intrasexual selection, where members of the one sex compete for mates, usually in the form of male fights or contests, or intersexual selection (mate choice) where certain individuals are found to be more attractive than others. In either case, some individuals leave more descendants than other individuals.

A male guppy, Image by Akwarium Foto [external site]

The guppy, Poecilia reticulata, is a small tropical fish, from the freshwater streams of Trinidad, known for their conspicuous and immensely varied male colour patterns. Mature males possess larger tails than females and a variety of polymorphic markings while females are of uniform colour. This sexual dimorphism (difference) is often indicative of sexual selection.

It is well established that male colour patterns are highly heritable and the basis of mate choice. Males court females incessantly, but females primarily choose whom to mate with. As a trait under sexual selection, the level of variation in male colour patterns is especially surprising as selection is expected to deplete variation, as only the males with few most appealing patterns will procreate. However, though their conspicuous colour patterns were more than likely the attribute that initially led to sexual selection studies in guppies, we are still unable to satisfactorily explain why such extreme levels of polymorphism persist.

In the simplest scenario, the balance between mutations introducing new variants and natural selection removing other variants determines the level of genetic variation. Antagonistic effects caused by conflicting forms of selection may maintain greater than expected variation as the trade-off could result in different combinations of variants of equal fitness. This is thought to be the case in guppies as it is well established that brightly coloured male guppies are favoured by females but are also at greater risk from predators. Frequency-dependent mate choice by females, where they prefer rare or novel (infrequent) males, is a common proposal because it has the potential to maintain extensive variation. The suggestion is that females prefer males who have unusual colour patterns, a phenomenon known as the “rare-male effect”.

There have been few studies on frequency-dependent mate choice in guppies. Farr1 and Hughes et al.² both found a female preference for novel or unfamiliar (‘unfamiliar’ meaning new to the female but not necessarily rare in nature) males in guppies, while Kelley. et al³ found a male preference for unfamiliar females. We tested for preferences for an unfamiliar mate as a factor contributing to the maintenance of the variation in male colour patterns. A preference for unfamiliar males is argued to be equivalent to a preference for rare males. Though female mating preferences in guppies are considered more significant, a male preference for unfamiliar females would also contribute to high levels of variation.

Our experimental protocol was similar to that of Hughes et al.² We familiarized males and females and then conducted behaviour trials with familiar and unfamiliar individuals. Female responses to male sigmoid displays were scored according to how much interest the female seemed to show. This method allowed us to compare the number of displays by the unfamiliar and familiar males to determine if males preferred unfamiliar females. It also allowed us to compare the scores of the displays to determine if females preferred unfamiliar males.

Based on earlier studies, we expected to find a female preference for unfamiliar males due to the ‘rare-male effect’. Yet, we found no significant difference in female response to unfamiliar and familiar males. Since none of our fish were allowed to mate prior to the trials, we were less surprised to find no male preference for unfamiliar females as there was no biological advantage for males discriminating against females they have not previously mated with. These results indicated that familiarity alone was not important in mate choice. Thus a preference for unfamiliar mates could not explain the extreme variation in male colour patterns. Alternatively, it is possible that we did not allow sufficient time for the fish to become familiarized. However, it is unlikely that wild populations of guppies would experience such an intensive familiarization. Thus, it would still be unlikely that familiarity is an important component of mate choice. In either case, a preference for unfamiliar mates cannot explain the extreme variation in male colour patterns.

This result suggests the ‘rare-male effect’ may not be as significant as once believed since the quantity of variation in itself means every male is likely to be rare under some criteria. So, my summer’s effort did not yield an earthshaking discovery. However, I did learn that careful experimentation, like what I was involved in, can challenge specialised scientific theories.

References

1. Farr, J. A. (1977). Male rarity or novelty, female choice behaviour, and sexual selection in the guppy, Poecilia reticulata. Evolution, 31, 162-168

2. Hughes, K. A., Du, L., Rodd, F. H. and Reznick, D. N. (1999). Familiarity leads to female preference for novel males in the guppy, Poecilia reticulata. Animal Behaviour, 58, 907-916

3. Kelley, J L., Graves, J. A. and Magurran, A. E. (1999). Familiarity breeds contempt in guppies. Nature, 401, 661-662.

Further reading

Brooks, R. (2002). Variation in female mate choice within guppy populations: population divergence, multiple ornaments and the maintenance of polymorphism. Genetica, 116, 343-358

Houde, A. E. (1997). Sex, Color and Mate Choice In Guppies. Princeton University Press

Glossary

Heterozygote: A diploid organism with two different alleles of the one gene.

Homozygote: A diploid organism with two of the same alleles of the one gene.

Phenotype: The physical appearance resulting from the genotype.

Polymorphism: Variants, in this case, in the colour patterns of the male guppies.

Sigmoid display: The mating displays male guppies perform to attract mates.