Frequency-dependent selection as a mechanism maintaining the genetically based variation in male guppy colouration
Wild guppies (Poecilia reticulata) exhibit one of the most striking examples of genetic polymorphism among animals. In local populations, there may be almost as many different male colour patterns as there are males, yet colour pattern is genetically determined. Previous work suggests that rare or novel males have an advantage in attracting mates and avoiding predators, possibly leading to negative frequency-dependent selection.
Another hypothesis consistent with these results is that males that are similar or identical to other males in colour pattern are at a disadvantage due to “redundancy” (as opposed to an advantage of rarity) of their pattern. Using a combination of field and laboratory studies, we are testing for frequency-dependent mating and survival advantages that could maintain genetic variation in male colour pattern. We have found that males with rare colour patterns do indeed have a survival advantage (Olendorf et al. 2006); one of our goals is to examine factor(s) that could contribute to this advantage: does it have to do with the predator’s attack strategy? with the mate searching strategies of male guppies?
Collaborators: Kim Hughes, Florida State University Anne Houde,Lake Forest College (see Anne's webpage for information about her excellent book on guppies)
Publications: Olendorf, R & F.H. Rodd, D. Punzalan, A.E. Houde, C. Hurt, D.N. Reznick & K.A. Hughes. 2006. Frequency-dependent survival in natural guppy populations. Nature 441: 633-636 (pdf) Hughes, K.A., F.H. Rodd and D.N. Reznick. 2005. Genetic and environmental effects on secondary sex traits in guppies (Poecilia reticulata). Journal of Evolutionary Biology 18: 34-45 (pdf) Hughes, K.A., L. Du, F.H. Rodd and D.N. Reznick. 1999. Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulata. Animal Behaviour 58: 907-916 (pdf)
Sensory bias in poeciliids
Most female guppies (Poecilia reticulata) prefer males with large, bright orange spots (Endler & Houde 1995). This preference may provide females with information about the quality of potential mates (e.g. parasite load, sperm number) (Houde 1997, Pitcher 2005). However, this preference may have arisen originally as a sensory bias–male and female guppies forage on orange-coloured foods (e.g. fruit) and are attracted to orange outside a mating context (i.e. to orange-painted disks) (Rodd et al. 2002).
We have found that the strength of female preference for orange spots on males is tightly correlated, across ten populations, with the number of times females in these populations peck orange-coloured disks (Rodd et al. 2002, Grether et al. 2005).
These results show an association between a potential trigger of a mate choice preference and a sexually selected trait and support the ‘sensory bias’ hypothesis for the evolution of mating preferences. Did the guppy mate choice preference for orange spots on males arisen as a by-product of foraging on orange fruit? We are using several approaches to answer this question.
- First, the simplest, proximate explanation for the between-population variation in responsiveness to orange in both mating and non-mating contexts is that there is between-population variation in visual sensitivity to orange. We are characterizing the relative sensitivity of guppies to different wavelengths, with a focus on long wavelengths (especially orange), using phenotypic assays (we plan to start testing guppies in an optomotor apparatus). Cam Weadick, my former PhD student (co-advised with Belinda Chang) was characterizing variation in guppy visual pigment proteins, the opsins, at the molecular level.
- Second, we are asking whether natural selection could be acting on orange vision in guppies mediated either through the general ambient colour characteristics of the environment or, specifically, through foraging ability.
- Third, responsiveness to orange in some populations may be reduced if females are paying costs, as a side effect of this attraction to orange, by associating too much with males. One potential cost for females includes parasite transmission.
- Fourth, is it possible that females prefer males with rare colour patterns because they have a general attraction to novelty? Is there an ancestral sensory bias towards orange among poeciliids in general?
Plans include phylogenetic comparative analyses to look at the possible origin(s) of this sensory bias and its potential role throughout the poeciliid family. To try to determine the origin of this preference for orange, we began by measuring the responsiveness of other poeciliid species to coloured disks.
To date, we have tested three molly species, closely related to the guppy (Poecilia velifera, P. petenensis, P. mexicana), and the more distantly related least killifish (Heterandria formosa) to coloured disks. Two of the molly species, like guppies, have a bias towards orange/red coloured objects in a non-mating context. The third molly species, which did not respond to the orange/red disks and has the lowest levels of female mating preference of the mollies measured thus far, did respond to green disks. H. formosa, which did not show a strong response to the orange disks, have little orange coloration and no courtship display.
Future studies will involve mapping onto the phylogeny for the family (e.g. Hrbek et al. 2007): responsiveness to colours in a non-mating context; scores of male colouration (and reproductive behaviour (courtship or not); and aspects of the habitat that could influence signal (male colouration) efficiency (e.g. water colour, turbidity, habitat complexity, substrate colour (Endler 1992).
Collaborators: Anna Price, U of Toronto Margaret Ptacek, Clemson University Shala Hankison, Clemson University Greg Grether, UCLA Gita Kolluru, CalPoly
Publications: Grether, G. F. Kolluru, G.R. Rodd, F.H. De La Cerda, J. Shimazaki, K. 2005. Carotenoid availability affects the development of a colour-based mate preference and the sensory bias to which it is genetically linked. Proc. R. Soc. B. 272: 2181-2188(pdf) Rodd, F.H., K.A. Hughes, G. Grether, C.T. Baril. 2002. A possible non-sexual origin of a mate preference: are male guppies mimicking fruit? Proc. R. Soc. B. 269:475-481(pdf)
Plasticity in life history traits and behaviour
I also have an interest in phenotypic plasticity in reproductive strategies: life history traits and sexual behaviour. We study the ways in which individuals adjust their reproductive strategies in response to the behaviour and population demography (e.g., sex ratio, density) of conspecifics, to predation risk, and whether those strategies are adaptive. For example, female H. formosa, another livebearing poeciliid, provide nutrients to their offspring throughout development and, in some populations, this species lives at extremely high densities. Do females of this species, as theory predicts, produce larger offspring at higher densities? And if so, what are the advantages of a larger size at birth?
Collaborators on the Heterandria formosa project on plasticity in offspring size in response to population density: Joe Travis, Florida State University Jeff Leips, UMBC
Publications: Gosline, A.K. and F.H. Rodd. 2007. Predator-induced plasticity in guppy (Poecilia reticulata) life history traits. Aquatic Ecology. DOI 10.1007/s10452-007-9138-7(pdf) Rodd, F.H., D.N. Reznick and M.B. Sokolowski. 1997. Phenotypic plasticity in the life history traits of guppies: response to social environment. Ecology 78:419-433(pdf) Rodd, F.H. and M.B. Sokolowski. 1995. Complex origins of variation in the sexual behaviour of male Trinidadian guppies (Poecilia reticulata):interactions among social environment, heredity, body size, and age. Animal Behaviour 49:1139-1159 pdf)