Mate choice

10.4.2 Mate choice

Benefits of mate choice

Mate choice can be defined as any behaviour that increases the likelihood of mating with certain members of the opposite sex. Theories to explain the evolution of mate preferences can be divided into those yielding either genetic or non-genetic benefits (reviewed in Andersson 1994). The magni- tude of the benefits of choosiness will be propor- tional to the amount of variation in mate quality of the opposite sex (Owens and Thompson 1994; Johnstone et al. 1996).

The nature of potential genetic benefits has been much debated. According to Fisherian models (Fisher 1930) male ornaments are merely arbitrary traits that females find attractive. Orna- mented males thus have a high mating success and selective females gain through the production of attractive sons, so long as ornament expression is heritable. If female preference is also heritable, the ornamental trait and the preference will become associated in the offspring. This may lead to a self- reinforcing runaway process causing exaggeration of the ornamental trait. Evidence has been found for positive genetic correlations between female preferences and preferred male ornaments, such as in the three-spine stickleback (Bakker 1993). However, a positive genetic correlation between preference and ornament is predicted not only by Fisherian models but also by good genes models (below).

Good genes models, also known as viability in- dicator models, suggest that male ornament ex- pression signals the genetic quality of the bearer. By mating with males with extravagant orna- ments females gain indirect benefits through the production of offspring that grow more quickly, are more viable or are more fecund (carrying ‘good genes’). In most of these models, the trait is thought to be costly to produce or carry and only males of high quality can afford to have such a ‘handicap’ (Zahavi 1977). Thus, the handicap will act as an honest signal. A special case of this was proposed by Hamilton and Zuk (1982), suggesting that ornamental traits reflect the bearer’s re-

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sistance to parasites. A mechanism for how this might work was suggested by Folstad and Karter (1992) in their immunocompetence handicap model: the primary androgenic hormone, testos- terone, stimulates ornament expression at the same time as it interferes with the immune sys- tem. Thus, only high-quality healthy males would afford a high ornament expression associated with high androgen levels. Another type of genetic benefit comes from mating with an individual hav- ing a very different genotype, thereby obtaining complementary genes for the offspring (Jennions 1997). Whether this occurs in fish is an open question. Wedekind (1996) speculated that this might explain strong individual preferences among female roach.

Mating preferences may also have evolved through direct selection. Here, females gain direct (non-genetic) fitness benefits that increase their survival or reproductive success. Examples of direct benefits are access to a safe and resource- rich territory, nuptial gifts and provision of high- quality parental care (reviewed in Andersson 1994).

Numerous studies of mate choice have been carried out on fish, which provide good model systems that are often suitable for experimental manipulations. Many of these studies have been concerned with what type of benefits females might gain through their choice of mate. Whether females are able to pick a mate with good genes is still a controversial question (Andersson 1994). One example from fish comes from an experiment on guppies, where Reynolds and Gross (1992) (Fig. 10.3) found that matings with preferred large males produced offspring that had a higher growth rate and daughters with a higher reproductive suc- cess. However, recent findings on the same species suggest that another component of male attrac- tiveness, their ornamentation, may be related to lower offspring survival (Brooks 2000). In a pipefish, both male and female choice resulted in higher offspring quality in terms of ability to es- cape predation. In addition, female choice resulted in higher offspring growth rate (Sandvik et al. 2000). There might, however, be other explana- tions than good genes for these results, such as

differential allocation into eggs or parental care depending on the attractiveness of the partner (reviewed in Sheldon 2000). Several studies, for example on guppies (Houde and Torio 1992) and

20.0 22.5 25.0 Male size (mm)

Female preference (no. of displays)

Daughter growth

(mm)

Daughter reproduction

(mg offspring)

Fig. 10.3 Results from an experiment designed to test for potential genetic benefits in female mate choice by Trinidadian guppies. (a) Females prefer larger males (total length). (b) These same males sire faster-growing daughters (total length at a standard age of 78 days). (c) These daughters have higher reproductive output over their first two broods (sum of dry weight at birth). Each data point represents the mean preference or offspring performance of two females tested per male. The scales are log-transformed with labels in original units. (Source: from Reynolds and Gross 1992.)

Behavioural Ecology of Reproduction

sticklebacks (Milinski and Bakker 1990, but see phus breviceps , heavily parasitized females were Fitzgerald et al. 1993), have shown that fish avoid less selective than less parasitized females, appar- parasitized mates. This preference might render ently because they had depleted energy stores and genetic benefits in terms of parasite resistance were in poor physical condition (Poulin 1994; genes passed on to the offspring (Hamilton and Barber and Poulin, Chapter 17, this volume). In Zuk 1982). However, females may also gain direct several experiments, increased predation risk has benefits by avoiding contagious parasites or by been found to result in decreased choosiness (e.g. avoiding males that are too sick to provide ade- Forsgren 1992; Berglund 1993). Although choosi- quate parental care (see also Barber and Poulin, ness apparently is very cost sensitive and may Chapter 17, this volume).

disappear if search costs are high, females may be

Evidence for direct benefits of mate choice willing to pay some costs to obtain preferred through high-quality parental care comes from mates. In redlip blennies, Ophioblennius atlanti- several correlational studies (e.g. Downhower and cus , some females travelled quite extensive dis- Brown 1980; Côté and Hunte 1989). Choice for tances in search of mates, enduring severe attacks parental ability has also been confirmed in experi- from damselfish whose territories they crossed in ments where confounding variables such as female the process. However, these females obtained quality and clutch size were controlled (Knapp and higher quality mates than females with a more re- Kovach 1991; Forsgren 1997a). In the study of the stricted search (Reynolds and Côté 1995). In the bicolor damselfish, Stegastes partitus, by Knapp damselfish Stegastes nigricans, females changed and Kovach (1991), females were apparently able to the number of spawning visits depending on the select good fathers by using courtship intensity as distance to the males’ territories, probably in order

a cue. to minimize costs in terms of intrusions to their own territories and attacks from heterospecifics (Karino and Kuwamura 1997).

Mate sampling and costs of mate choice

Several models of search behaviour have been de- veloped to describe how animals should search for

Ornaments and other choice cues

mates (see Luttbeg 1996 and references therein). Many examples from fish show that females However, very few empirical studies on taxa other base their mate choice on male characteristics than birds have been devoted to this problem (re- (reviewed in Andersson 1994). Examples of male viewed in Gibson and Langen 1996). Female sand traits that may have evolved through female gobies appear to use a threshold criterion when se- choice include coloration (Milinski and Bakker lecting potential partners (Forsgren 1997b). Males 1990; Houde 1997), elongated fins (Bischoff et al. were inspected sequentially until one advertising 1985; Basolo 1990), body size (Côté and Hunte above a certain threshold courtship intensity was 1989; Reynolds and Gross 1992) and courtship dis- encountered and mating occurred. In the bicolour plays (Knapp and Kovach 1991). If these are honest damselfish (Knapp 1993) and the blenny Aid- signals of male quality, only high-quality males ablennius sphynx (Kraak and van den Berghe should be able to develop and carry highly elabo- 1992), females seemed to assess the success of rated versions of the traits (Zahavi 1977). Elaborate earlier laid eggs and avoided nests where eggs had traits can indeed be costly, as evidenced by the disappeared.

well-studied colour ornaments of male guppies

Search costs should reduce choosiness (reviewed in Endler 1995; Houde 1997; see also (Crowley et al. 1991) and several studies of fish Olson and Owens 1998 for a discussion of costs have demonstrated this. In an experiment on stick- of carotenoid colours). Also, in the Amarillo fish lebacks, females became less choosy if time costs elaborate traits are costly, as males with a mor- and energy expenditure were increased (Milinski phology attractive to females were more likely to and Bakker 1992). In the upland bullie, Gobiomor-

be captured by predatory snakes (Macías Garcia

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et al. 1994). Honest signalling may work if the optimum trait expression is different for indi- viduals of different quality. This can come about if poor-quality males pay higher costs than high-quality males for a certain trait expression (Johnstone 1997). To date this has not been conclu- sively demonstrated in any fish. There are, how- ever, data supporting the idea that ornaments are expressed in a condition-dependent way. For ex- ample, parasitized males have been found to de- velop a less bright carotenoid-based breeding coloration in sticklebacks (Milinski and Bakker 1990) and guppies (Houde and Torio 1992). Fe- males may also gain reliable information from cues that are honest by design rather than through costs (Hasson 1997), such as body size or visible parasites.

Females may also base their choice on aspects other than the male himself. Many fish have resource-based breeding systems, with males de- fending a spawning site. Without experimental manipulations it is often difficult to assess the im- portance of territory and male characteristics in mate choice, although there are studies indicating that the breeding site, in addition to male charac- teristics, is an important cue in mate choice (e.g. Kodric-Brown 1983). This was also the conclusion from an experiment with the river bullhead (Bisazza and Marconato 1988). In European bitter- ling, Rhodeus sericeus, females base their initial interest in males on the male’s courtship display, but the final spawning decision is based on the quality of spawning site that the male is defending (Candolin and Reynolds 2001). These fish spawn in living freshwater mussels (Unionidae) and females prefer mussel species that yield the highest sur- vival to their embryos (Mills and Reynolds 2002). In a removal experiment conducted in the wild, Warner (1988a) demonstrated that female blue- head wrasse chose particular spawning sites in- stead of male characteristics. Also, elaborate nest constructions may be attractive themselves (e.g. Jones and Reynolds 1999; Östlund-Nilsson 2001). An extreme form of extrabodily ornaments are found in some cichlids in the African rift lakes, where males construct impressive sand bowers to attract females (McKaye et al. 1990). As mentioned

in Section 10.3.3, females of several different fish prefer to spawn in nests already containing eggs from other females. Several hypotheses have been proposed to explain this, including mate choice copying, a predator dilution effect and high parental investment (see Jamieson 1995). An in- creased egg survival, resulting from the two latter mechanisms, might be a more likely explanation than mate choice copying (Jamieson 1995; Forsgren et al. 1996b).

It is not only males who carry extravagant orna- ments; females of many species are conspicuous in one way or another. In many fish, for example, fe- males are brightly coloured. The function of fe- male ornaments in species with conventional sex roles (see Section 10.4.3) is poorly understood in general, and most of our knowledge comes from studies on birds (Amundsen 2000). Traditionally, female ornaments have been assumed to be func- tionless, existing solely because of a genetic corre- lation between male and female traits, in cases where both sexes have similar ornamentation. Al- ternatively, female ornaments may have been se- lected for by male choice or female competition (see Section 10.4.3). Recent experiments have demonstrated that males are attracted to colour- ful females in both sex-role reversed pipefish (Berglund and Rosenqvist 2001) and conventional- role gobies (Amundsen and Forsgren 2001). If female ornaments have evolved through male choice for direct or indirect benefits, the orna- ments should provide information about female quality. There is evidence from Arctic charr, Salvelinus alpinus , that the intensity of the carotenoid-based coloration is informative of immunocompetence or health in both sexes (Skarstein and Folstad 1996).

Interactions between male competition and female choice

Males successful in male competition should be in better condition and might also have higher viabil- ity than unsuccessful males. It is therefore gen- erally believed that females should benefit by mating with winners of male competition (re- viewed in Berglund et al. 1996). Thus, female Males successful in male competition should be in better condition and might also have higher viabil- ity than unsuccessful males. It is therefore gen- erally believed that females should benefit by mating with winners of male competition (re- viewed in Berglund et al. 1996). Thus, female