Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections

Abstract

'Good genes' models of sexual selection suggest that elaborate male sexual ornaments have evolved as reliable signals of male quality because only males of high genetic viability are able to develop and maintain them. Females benefit from choosing such individuals if quality is heritable. A key prediction is that the offspring of males with elaborate mating displays will perform better than those of less elaborate males, but it has proved difficult to demonstrate such an effect independently of the effects of differences in parental investment. We tested for 'good genes' linked to male ornamentation in the three-spined stickleback Gasterosteus aculeatus using in vitro fertilization to generate maternal half-siblings, which were raised without parental care. Maternal half-siblings sired by brightly coloured males grew less quickly than half-siblings sired by dull males but were more resistant to a controlled disease challenge. Among the offspring that became infected, those with brighter fathers had higher white blood cell counts. This suggests that highly ornamented males confer disease resistance on their offspring. The association with reduced growth suggests a mechanism for the maintenance of heritable variation in both disease resistance and male sexual coloration.

Calling Is an Honest Indicator of Paternal Genetic Quality in Poison Frogs

“…The ''good genes'' hypothesis suggests that male advertisement displays function as a reliable signal of genetic quality. By selecting males with extravagant secondary sexual characters (i.e., of high genetic quality) females may obtain fitness benefits mediated via enhanced offspring viability (Zahavi 1975(Zahavi , 1977Andersson 1982;Ryan et al 1982;Kirkpatrick and Ryan 1991;Petrie and Williams 1993;Proehl and Hodl 1999;Doty and Welch 2001;Kokko et al 2003).In support of this theory there is a large body of evidence for benefits (i.e., fitter offspring) to females for choosing a male based on secondary sexual characters (Hamilton and Zuk 1982;Hillgarth 1990;Potts et al 1991;Moore 1994;Hasselquist et al 1996;Sheldon et al 1997;Alatalo et al 1998;Hoikkala et al 1998;Welch et al 1998;Wilkinson et al 1998;Møller and Alatalo 1999;Sandvik et al 2000;Barber et al 2001;Kotiaho et al 2001;Wedekind et al 2001;Sheldon et al 2003). In their meta-analysis of published studies of good genes effects in sexual selection Møller and Alatalo (1999) found a weak but significant correlation between the expression of male secondary sexual traits and offspring survival, a finding in accordance with the hypothesis that females may obtain genetically based viability benefits from their choice.…”

Sire attractiveness influences offspring performance in guppies

“…Recent studies that have adopted artificial fertilization techniques have provided some of the most compelling evidence to date for the good-genes hypothesis (Welch et al 1998;Barber et al 2001;Parker 2003;Sheldon et al 2003). Among these, Sheldon et al (2003) reported that under certain predation conditions sire coloration (and therefore presumably male attractiveness) influenced the susceptibility of juvenile moorfrogs to predation by water beetles.…”

“…Artificial insemination provides a potential method for controlling such effects because it uncouples mate choice from copulation, thus preventing the direct assessment of male attractiveness by females. For example, in vitro fertilization techniques for external fertilizers (see Welch et al 1998;Barber et al 2001;Sheldon et al 2003) and in vivo artificial insemination for internal fertilizers (Parker 2003) have facilitated powerful tests of the good-genes hypothesis in recent studies. Here, we also use artificial insemination to test whether early offspring performance in juvenile guppies (Poecilia reticulata) is related to paternal attractiveness.…”

A receiver bias in the origin of three–spined stickleback mate choice

“…As discussed previously, red coloration in male sticklebacks appears honestly to signal direct and indirect fitness benefits to female receivers (e.g. Milinski & Bakker 1990;Barber et al 2001;but see Candolin 1999). Zahavi (1975) proposed that a sexual signal must impose a fitness cost on the signaller to be reliable.…”

“…In at least one population, male three-spined sticklebacks adorn their nests with red objects, when given the opportunity, which has the effect of increasing their reproductive success (Ö stlundNilsson & Holmlund 2003). Red breeding coloration in the three-spined stickleback correlates with male condition (Milinski & Bakker 1990), offspring parasite resistance (Barber et al 2001), courtship effort (Bakker & Milinski 1991), nest defence during parental care (McKinnon 1996) and mating success (Bakker & Mundwiler 1994;Rowland 1994). Thus, the degree of red coloration of male sticklebacks appears to signal both direct and indirect benefits to females, at least in those populations where correlations exist.…”