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First published online May 26, 2006
Journal of Experimental Biology 209, 2368-2376 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02183

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Phenotypic plasticity, sexual selection and the evolution of colour patterns

Trevor D. Price

Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637, USA

View larger version (11K): [in a new window]   Fig. 1. The adaptive surface model of the contribution of phenotypic plasticity to successful colonization of a new environment. In this example the bold line is the adaptive surface (i.e. mean fitness curve). The solid thin line is the phenotypic distribution. For illustration, an environmental change is assumed to affect phenotypic plasticity without affecting the mean fitness curve, and to cause a shift in the mean of the phenotypic distribution without changing the variance. Broken lines indicate three levels of plasticity, from small (1) to moderate (2) to large (3). In (1), plasticity is insufficient to bring the population into the realm of attraction of the higher peak. This then leads to genetic evolution back towards the first peak, a process termed genetic compensation (Grether, 2005). In (2), plasticity brings the population into the realm of attraction of the higher peak, and there is then directional selection resulting in genetic change. In (3), plasticity is large, and the population is immediately centered under the higher peak; in this case there is no genetic change. A moderate amount of plasticity (2) is thus optimal for genetic assimilation.

View larger version (122K): [in a new window]   Fig. 2. Effects of an absence of carotenoids in the diet on the plumage colouration of male house finches from Michigan. The orange male was fed a carotenoid restricted diet (Hill, 1994b). Photo courtesy of Geoffrey E. Hill and David Bay.

View larger version (48K): [in a new window]   Fig. 3. (A) Great tit Parus major, from Holland. (B) Great tit raised in captivity. This individual resembles closely the phenotype of the subspecies of great tit that breeds in India (see Gompertz, 1968). Photographs courtesy of the Archives Netherlands Institute of Ecology, provided by A. J. van Noordwijk. (C) Chroma score (mean ± s.e.m.) (i.e. colour saturation) of whole great tit Parus major broods raised in deciduous and coniferous woodland near Trondheim, Norway (after Slagsvold and Lifjeld, 1985). Colour was measured on the yellow breast of young chicks at age 10–15 days. Chroma score is in arbitrary units, estimated by comparison to a colour guide. Triangles, broods transferred as eggs from one habitat to the other; squares, broods not transferred. Sample sizes are from top: 1 (hence no standard error on this point), 7, 3 and 6 broods. In a two-way ANOVA comparing locality of origin with locality of rearing, there is a significant effect of rearing environment (F1,13=7.5, P=0.02) but none of laying environment (F1,13=0.01, P=0.9).

View larger version (62K): [in a new window]   Fig. 4. Geographical variation in colour patch size of house finches, Carpodacus mexicanus. The male on the left with the large patch is from Michigan (as in Fig. 2), that on the right with the smaller patch from Guerrero in Mexico (see Hill, 1993). Photo courtesy of Geoffrey E. Hill and David Bay.

View larger version (37K): [in a new window]   Fig. 5. Peak shift model for the evolution of the colour patch in male house finches, following published descriptions (Hill, 1993; Hill, 1994b). The Michigan population (1) is inferred to be ancestral, with a large red patch (see Fig. 4). Establishment in Mexico is thought to have resulted in fewer carotenoids in the diet, resulting in a large pale patch as a phenotypically plastic response (2; see Fig. 2). Subsequent selection to increase patch brightness resulted in genetic evolution of small patch size (3) as in the Mexican population (Fig. 4).

View larger version (40K): [in a new window]   Fig. 6. Examples of melanin pigment patterns produced by experimental manipulation (A–D) and computer simulation (E,F). (A,B) Ornamental feather from the neck region of a male Brown Leghorn chicken receiving 1.5 mg of a subcutaneous injection of thyroxin every sixth day during growth of the feather (Lillie, 1932) (A); (B) control feather from the same region. (C,D) Normal feather from the wing covert of a short eared owl (C), and (D) a feather from the same covert induced to grow after removal of the thyroid gland [from Voitkevich (Voitkevich, 1966), p.183]. (E,F) Two patterns produced in computer simulations of diffusion and interactions between two molecules (`activator' and `inhibitor') on a growing feather (Prum and Williamson, 2002). The activator stimulates production of both activator and inhibitor. Inhibitor diffuses faster than, and inhibits, activator. Dark areas are locations where the activator is above a certain concentration. One important difference between the two simulations is that the diffusion rate of inhibitor is higher when the longitudinal patch is produced. Both these patterns are commonly observed across feather tracts of different species of birds (Prum and Williamson, 2002).