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Mutation and Sexual Selection: a Test Using Barn Swallows from Chernobyl

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Mutation and Sexual Selection: a Test Using Barn Swallows from Chernobyl Evolution, 57(9), 2003, pp. 2139±2146 MUTATION AND SEXUAL SELECTION: A TEST USING BARN SWALLOWS FROM CHERNOBYL A. P. MùLLER1 AND T. A. MOUSSEAU2 1Laboratoire de Parasitologie Evolutive, CNRS UMR 7103, Universite Pierre et Marie Curie, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France E-mail: [email protected] 2Department of Biological Sciences, University of South Carolina, Columbia, South Carolina 29208 E-mail: [email protected] Abstract. Secondary sexual characters have been hypothesized to be particularly susceptible to the deleterious effects of mutation because the expression of such characters is usually in¯uenced by many more metabolic pathways than are ordinary morphological characters. We tested this hypothesis using the elevated mutation rates in the barn swallow (Hirundo rustica) of the Chernobyl region of Ukraine as a model system. A great deal is known about the relative importance of different characters for male mating success in this species. The importance of phenotypic characters for male mating success was quanti®ed based on a long-term study of a Danish breeding population, by expressing phenotypic differences between mated and unmated males as the difference between log-transformed mean values. For ®eld samples from Ukraine we likewise expressed the difference in male phenotype between individuals living in a relatively uncontaminated area and individuals from the Chernobyl region as the difference between log-trans- formed mean values. The standardized difference in male phenotype between the two regions in Ukraine for the 41 different characters was strongly positively correlated with the standardized difference in male phenotype between mated and unmated males from Denmark. The standardized difference in male phenotype between the two regions in Ukraine was signi®cantly positively associated with sexual size dimorphism. However, the standardized difference in male phenotype between mated and unmated males was a much better predictor of standardized difference in male phenotype between the two regions in Ukraine than was the standardized difference in sexual size dimorphism, expressed as the difference between log-transformed mean values for males and females. These ®ndings are consistent with the hypothesis that traits most important for sexual selection are particularly susceptible to the effects of deleterious mutations. Key words. Antioxidants, Chernobyl, condition dependence, Hirundo rustica, mate choice, mutation, sexual selection. Received January 20, 2003. Accepted March 18, 2003. The advantages of strong mate preferences in sexual se- viability by 20% or more (Charlesworth 1987; Kondrashov lection remain largely undetermined (Andersson 1994). There 1988; Rice 1988; Lynch et al. 1999). Such effects may ac- is good evidence of direct, material bene®ts of mate choice count for the small, but highly signi®cant heritability of ®t- in many taxa, but others show direct bene®ts generally being ness (Burt 1995) and ®tness components (Mousseau and Roff of little or no importance (reviewed in Mùller and Jennions 1987; Roff and Mousseau 1987). 2001). Although there is ample evidence for females obtain- We quanti®ed the effects of mutation on phenotype by ing genetic bene®ts for their offspring (reviewed in Mùller expressing the difference in phenotype between male barn and Alatalo 1999), the mechanisms generating such bene®ts swallows (Hirundo rustica) from a little-contaminated region remain illusive. Although mutation-selection balance likely in Ukraine (Kanev) and conspeci®cs from the Chernobyl re- plays a role in maintaining additive genetic variance in ®tness gion, which has high levels of radioactive contamination and the expression of secondary sexual characters, whether (mainly Cs 137 and Sr 90; Shestopalov 1996). Ellegren et such effects are suf®cient is unknown. A Fisherian mecha- al. (1997) reported an increase in germline mutation rates in nism of sexual selection could arise from biased mutations barn swallow microsatellite DNA by a factor of two to 10 affecting the expression of male secondary sexual characters when comparing families from Kanev with families from (Pomiankowski et al. 1991), allowing females to avoid mu- Chernobyl. Barn swallows from Chernobyl have markedly tants from inspection of male phenotype. Male secondary increased frequency of partial albinism in the plumage (El- sexual characters are exaggerated traits that for this reason legren et al. 1997; Mùller and Mousseau 2001). Previous are likely to be affected by many different metabolic path- studies have shown signi®cant parent-offspring resemblance ways. Therefore, mutations may more readily be assessed in partial albinism, indicating that such albinism is partly of from such characters than from ordinary phenotypic traits germline origin (Ellegren et al. 1997). Individuals with partial that are primarily in¯uenced by mutations through a single albinism are less likely to survive than other individuals (El- or few metabolic pathways. Similarly, biased mutation si- legren et al. 1997), and they generally have a smaller but multaneously differentially affecting viability and the ex- more variable phenotype (Mùller and Mousseau 2001). These pression of male traits may render continuous sexual selec- patterns of phenotypic variation are consistent with the hy- tion feasible (Iwasa et al. 1991). Both these ideas are based pothesis that radioactive contamination has increased the rate on the untested assumption that deleterious mutations con- of mutations, and that such mutations have deleterious ef- stantly reduce the expression of male traits and maximum fects. Thus, this area has the potential for providing insights viability. Estimates of the additive genetic variance in via- into the effects of mutation on sexual selection and other bility have suggested that deleterious mutations may reduce evolutionary phenomena. 2139 q 2003 The Society for the Study of Evolution. All rights reserved. 2140 A. P. MéLLER AND T. A. MOUSSEAU One aim of this study was to investigate the extent to which surements and subsequent banding. Our own ®eld measure- the phenotypic characters that vary in importance for male ments of radiation at the ground level using a hand-held mating success are susceptible to the deleterious effects of Inspector dosimeter (SE International, Inc., Summertown, mutation. We predicted that the standardized difference in TN) revealed average levels of radiation of 0.390 mR/h (SE male phenotype between mated and unmated males, re¯ected 5 0.317) at 14 breeding sites in the Chernobyl region. As a by the difference between log-transformed mean values, control area we used Kanev, about 220 km southwest of Kiev, should represent an estimate of the importance of a character which has a relatively low level of contamination. Mean lev- for sexual selection. Likewise, we expressed the standardized els of radiation were 0.025 mR/h (SE 5 0.002) at ®ve breed- phenotypic difference between individuals from the contam- ing sites. We studied barn swallows in the two study areas inated and the control area. If secondary sexual characters 10±29 June 1991 (A. P. Mùller), 16±24 June 1996 (A. P. were particularly susceptible to the effects of mutation, com- Mùller), 6±12 June 2000 (A. P. Mùller, T. A. Mousseau) and pared to other phenotypic characters, we would predict a 4±11 June 2002 (A. P. Mùller, T. A. Mousseau). positive association between standardized difference in male We captured barn swallows with mist nets across open phenotype with respect to mutation and standardized differ- doors and windows in farm buildings. This method is highly ence in phenotype with respect to male mating success. A ef®cient during the main breeding season since mark-recap- second aim of this study was to investigate the relationship ture studies have shown a capture probability of 98% (Mùller between sexual size dimorphism and effects of radiation on and SzeÂp 2002). phenotype. We standardized sexual size dimorphism as de- We measured a total of 41 phenotypic characters in adult scribed above. Sexual dimorphism evolves over extremely males and females from the two samples. Twenty morpho- long time periods (Lande and Arnold 1985), whereas females logical characters (beak length, beak width, beak depth, wing are supposed to assess phenotypic characters that currently length, wing asymmetry, tail length, tail asymmetry, length reveal bene®ts from mate choice (Andersson 1994). There- of central tail feathers, wingspan, wing area, wing loading, fore, we can predict that the standardized difference in phe- aspect ratio, tarsus length, keel length, feather tip width, notype related to mating success is mainly related to the feather base width, tip vane asymmetry, base vane asym- standardized difference in phenotype related to radiation, and metry, difference in width between tip and base, and body much less to the difference in phenotype related to sexual mass) were measured with a ruler, a digital caliper, or a Pesola size dimorphism. AG (Baar, Switzerland) spring balance as described in Mùller (1994a) and Mùller et al. (1995). Six color variables (chroma, MATERIALS AND METHODS hue, ultraviolet re¯ectance, lutein-based re¯ectance, visible light re¯ectance, and albinism) were measured as described Study Species in Camplani et al. (1999). Ten immunological and hemato- The barn swallow is an approximately 20-g aerial insec- logical variables (monocytes, heterophils, lymphocytes, eo- tivorous passerine bird (Mùller 1994a). Males arrive before
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