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Females prefer the scent of outbred males: good-genes-as-heterozygosity?

Ilmonen P, Stundner G, Thoss M, Penn DJ - BMC Evol. Biol. (2009)

Bottom Line: There is increasing interest to determine the relative importance of non-additive genetic benefits as opposed to additive ones for the evolution of mating preferences and maintenance of genetic variation in sexual ornaments.Females showed a significant preference for outbred males, and this preference was more pronounced among inbred females.Our study has implications for efforts to understand how mate choice can provide genetic benefits without eroding genetic diversity (lek paradox), and also conservation efforts to determine the fitness consequences of inbreeding and the maintenance of genetic diversity in small, inbred populations.

View Article: PubMed Central - HTML - PubMed

Affiliation: Konrad Lorenz Institute for Ethology, Austrian Academy of Sciences, Vienna, Austria. p.ilmonen@klivv.oeaw.ac.at

ABSTRACT

Background: There is increasing interest to determine the relative importance of non-additive genetic benefits as opposed to additive ones for the evolution of mating preferences and maintenance of genetic variation in sexual ornaments. The 'good-genes-as-heterozygosity' hypothesis predicts that females should prefer to mate with more heterozygous males to gain more heterozygous (and less inbred) offspring. Heterozygosity increases males' sexual ornamentation, mating success and reproduction success, yet few experiments have tested whether females are preferentially attracted to heterozygous males, and none have tested whether females' own heterozygosity influences their preferences. Outbred females might have the luxury of being more choosey, but on the other hand, inbred females might have more to gain by mating with heterozygous males. We manipulated heterozygosity in wild-derived house mice (Mus musculus musculus) through inbreeding and tested whether the females are more attracted to the scent of outbred versus inbred males, and whether females' own inbreeding status affects their preferences. We also tested whether infecting both inbred and outbred males with Salmonella would magnify females' preferences for outbred males.

Results: Females showed a significant preference for outbred males, and this preference was more pronounced among inbred females. We found no evidence that Salmonella infection increased the relative attractiveness of outbred versus inbred males; however, we found no evidence that inbreeding affected males' disease resistance in this study.

Conclusion: Our findings support the idea that females are more attracted to outbred males, and they suggest that such preferences may be stronger among inbred than outbred females, which is consistent with the 'good-genes-as-heterozygosity' hypothesis. It is unclear whether this odour preference reflects females' actual mating preferences, though it suggests that future studies should consider females' as well as males' heterozygosity. Our study has implications for efforts to understand how mate choice can provide genetic benefits without eroding genetic diversity (lek paradox), and also conservation efforts to determine the fitness consequences of inbreeding and the maintenance of genetic diversity in small, inbred populations.

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Female preferences measured as a) number of investigations, b) duration of investigations, c) number of visits and d) total duration separately for outbred (white symbol, n = 25) and inbred females (black symbol, n = 24). Data is pooled for trials in which both of the males were sham-infected or both infected, except for 1 c, in which the data is shown separately for trials with two sham-infected males (dashed line) and two infected males (solid line).
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Figure 1: Female preferences measured as a) number of investigations, b) duration of investigations, c) number of visits and d) total duration separately for outbred (white symbol, n = 25) and inbred females (black symbol, n = 24). Data is pooled for trials in which both of the males were sham-infected or both infected, except for 1 c, in which the data is shown separately for trials with two sham-infected males (dashed line) and two infected males (solid line).

Mentions: The results of GLM multivariate analysis showed that females preferred significantly outbred males over the inbred ones [Within-subjects effects, outbred (OB) versus inbred (IB) male: F = 3.0, d.f. = 4, Pdir = 0.02] measured by average of the four female preference behaviours, whereas neither the female inbreeding status (interaction term: OB versus IB male × female inbreeding status: F = 1.6, d.f. = 4, P = 0.19) or experimental infection (interaction term: OB vs IB × male infection status: F = 0.2, d.f. = 4, Pdir = 0.59) had no significant effects on female preference for outbred males. When using univariate models we found that females significantly preferred outbred compared to inbred males, measured by number of investigations (Table 1, Fig. 1a), duration of investigations (Table 2, Fig. 1b) and number of visits (Table 3, Fig. 1c), but not by total duration (Table 4, Fig. 1d). Interestingly, we found that preference for outbred males was somewhat stronger in inbred females versus outbred females (Figs 1a–d). This difference between inbred and outbred females was statistically significant for number of investigations (Table 1; Within-subjects contrasts, interaction term: OB versus IB male × female inbreeding status), and there was a similar, but non-significant trend for duration of investigations. Females' inbreeding status did not influence their preferences for number of visits (Table 3) or total duration (Table 4). When testing the inbred and outbred females separately, inbred females investigated the scent marks of outbred males significantly more often compared to the scent marks of inbred males (paired samples t-test, t = 4.50, d.f. = 23, Pdir = 0.0001), but outbred females did not show any clear preference (paired samples t-test, t = 0.79, d.f. = 24, Pdir = 0.44, Fig. 1a).


Females prefer the scent of outbred males: good-genes-as-heterozygosity?

Ilmonen P, Stundner G, Thoss M, Penn DJ - BMC Evol. Biol. (2009)

Female preferences measured as a) number of investigations, b) duration of investigations, c) number of visits and d) total duration separately for outbred (white symbol, n = 25) and inbred females (black symbol, n = 24). Data is pooled for trials in which both of the males were sham-infected or both infected, except for 1 c, in which the data is shown separately for trials with two sham-infected males (dashed line) and two infected males (solid line).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2698884&req=5

Figure 1: Female preferences measured as a) number of investigations, b) duration of investigations, c) number of visits and d) total duration separately for outbred (white symbol, n = 25) and inbred females (black symbol, n = 24). Data is pooled for trials in which both of the males were sham-infected or both infected, except for 1 c, in which the data is shown separately for trials with two sham-infected males (dashed line) and two infected males (solid line).
Mentions: The results of GLM multivariate analysis showed that females preferred significantly outbred males over the inbred ones [Within-subjects effects, outbred (OB) versus inbred (IB) male: F = 3.0, d.f. = 4, Pdir = 0.02] measured by average of the four female preference behaviours, whereas neither the female inbreeding status (interaction term: OB versus IB male × female inbreeding status: F = 1.6, d.f. = 4, P = 0.19) or experimental infection (interaction term: OB vs IB × male infection status: F = 0.2, d.f. = 4, Pdir = 0.59) had no significant effects on female preference for outbred males. When using univariate models we found that females significantly preferred outbred compared to inbred males, measured by number of investigations (Table 1, Fig. 1a), duration of investigations (Table 2, Fig. 1b) and number of visits (Table 3, Fig. 1c), but not by total duration (Table 4, Fig. 1d). Interestingly, we found that preference for outbred males was somewhat stronger in inbred females versus outbred females (Figs 1a–d). This difference between inbred and outbred females was statistically significant for number of investigations (Table 1; Within-subjects contrasts, interaction term: OB versus IB male × female inbreeding status), and there was a similar, but non-significant trend for duration of investigations. Females' inbreeding status did not influence their preferences for number of visits (Table 3) or total duration (Table 4). When testing the inbred and outbred females separately, inbred females investigated the scent marks of outbred males significantly more often compared to the scent marks of inbred males (paired samples t-test, t = 4.50, d.f. = 23, Pdir = 0.0001), but outbred females did not show any clear preference (paired samples t-test, t = 0.79, d.f. = 24, Pdir = 0.44, Fig. 1a).

Bottom Line: There is increasing interest to determine the relative importance of non-additive genetic benefits as opposed to additive ones for the evolution of mating preferences and maintenance of genetic variation in sexual ornaments.Females showed a significant preference for outbred males, and this preference was more pronounced among inbred females.Our study has implications for efforts to understand how mate choice can provide genetic benefits without eroding genetic diversity (lek paradox), and also conservation efforts to determine the fitness consequences of inbreeding and the maintenance of genetic diversity in small, inbred populations.

View Article: PubMed Central - HTML - PubMed

Affiliation: Konrad Lorenz Institute for Ethology, Austrian Academy of Sciences, Vienna, Austria. p.ilmonen@klivv.oeaw.ac.at

ABSTRACT

Background: There is increasing interest to determine the relative importance of non-additive genetic benefits as opposed to additive ones for the evolution of mating preferences and maintenance of genetic variation in sexual ornaments. The 'good-genes-as-heterozygosity' hypothesis predicts that females should prefer to mate with more heterozygous males to gain more heterozygous (and less inbred) offspring. Heterozygosity increases males' sexual ornamentation, mating success and reproduction success, yet few experiments have tested whether females are preferentially attracted to heterozygous males, and none have tested whether females' own heterozygosity influences their preferences. Outbred females might have the luxury of being more choosey, but on the other hand, inbred females might have more to gain by mating with heterozygous males. We manipulated heterozygosity in wild-derived house mice (Mus musculus musculus) through inbreeding and tested whether the females are more attracted to the scent of outbred versus inbred males, and whether females' own inbreeding status affects their preferences. We also tested whether infecting both inbred and outbred males with Salmonella would magnify females' preferences for outbred males.

Results: Females showed a significant preference for outbred males, and this preference was more pronounced among inbred females. We found no evidence that Salmonella infection increased the relative attractiveness of outbred versus inbred males; however, we found no evidence that inbreeding affected males' disease resistance in this study.

Conclusion: Our findings support the idea that females are more attracted to outbred males, and they suggest that such preferences may be stronger among inbred than outbred females, which is consistent with the 'good-genes-as-heterozygosity' hypothesis. It is unclear whether this odour preference reflects females' actual mating preferences, though it suggests that future studies should consider females' as well as males' heterozygosity. Our study has implications for efforts to understand how mate choice can provide genetic benefits without eroding genetic diversity (lek paradox), and also conservation efforts to determine the fitness consequences of inbreeding and the maintenance of genetic diversity in small, inbred populations.

Show MeSH
Related in: MedlinePlus