S22.2: Sexual selection and colony formation

Biology Department, York University, North York, Ontario M3J 1P3, Canada, fax 416 736 5989, e-mail rwagner@yorku.ca

The prevalence of colonial breeding remains an enigma in evolutionary ecology (Danchin & Wagner 1997). High density breeding always creates costs, such as increased aggression, parasite transmission and infanticide (Alexander 1974; Wittenberger & Hunt 1985; Siegel-Causey & Kharitonov 1990) and the traditional approach to studying coloniality has been to identify benefits that might outweigh such costs. This approach has produced a large body of evidence that certain benefits accrue from high density nesting. Two benefits in particular have been well documented: reduced predation (Darling 1938; Hoogland & Sherman 1976; Birkhead 1977) and enhanced food finding (Ward & Zahavi 1973; Brown & Bomberger Brown 1996; Buckley 1996). Despite such advances, however, decades of research have not led to the identification of general mechanisms that produce breeding aggregations.

A major reason for this impasse may be that the debate over why birds breed densely in colonies has been dominated by the assumption that coloniality is produced exclusively by natural selection: the benefits of food-finding and reduced predation affect the survival of adults and offspring. While these benefits have been studied in great detail, the role of sexual selection in colony evolution has, until recently, been almost entirely neglected. Considering the enormous potential for social interaction in dense colonies, in which large numbers of sexually active males and females breed in very close proximity, it seems surprising that little attention has been paid to the possibility of a causal link between sexual selection and colony formation. With a new surge of interest in sexual selection (Borgia 1988; Andersson 1994; Møller 1994; Ligon 1998), it may now seem obvious to consider such a link. However, such a connection had been, until recently, far from obvious. The historical reason for this oversight stems mainly from the hitherto reasonable assumption that sexual selection operates only weakly among monogamous species because of the apparent lack of variation in male mating success. However, numerous behavioural studies of marked birds, combined with DNA fingerprinting, have revealed that breeding partners often copulate outside of the pair bond (Birkhead & Møller 1992). The prevalence of ‘ extra-pair copulation’ (EPC) typically results in skews in male reproductive success that had, until now, been invisible. Consequently, it has suddenly become apparent that sexual selection operates much more intensely in monogamous mating systems than had previously been thought (Møller 1992). Traditionally, monogamy had been defined as an exclusive mating relationship between one male and one female that raise offspring together. However, monogamy is now coming to be seen in the more limited context of male-female cooperation in raising offspring, without assuming whether the male partner sires the brood. This system of biparental care needs to be viewed separately from the genetic mating system, which is defined by copulations and fertilisations (Gowaty 1985; Westneat et al., 1990). When the genetic mating system is viewed independently, many monogamous species are actually quite similar to promiscuous species in that male mating success is often skewed.

The notion that sexual selection might be linked to colony formation has previously been suggested in general terms by workers proposed that it is easier to find mates in colonies (Hamilton 1971; Alexander 1974; Burger & Gochfeld 1990). Draulans (1988) specifically compared heron colonies to leks because aggregated males display to females, but he also noted that a colony is not a lek because herons are monogamous and provide parental care, whereas males of lekking species do not. Morton et al. (1990) noted that certain males benefited from coloniality by fertilising the mates of other males, and suggested that this benefit could promote coloniality. Wagner (1993; 1997) incorporated female mating strategies in the ‘ hidden lek’ hypothesis which predicts that when monogamous birds pursue extra-pair copulations, the same mechanisms that produce leks operate. Just as the pursuit of promiscuous copulations by females in lekking species causes males to aggregate into display arenas, the pursuit of extra-pair copulations by monogamous females is predicted to produce aggregations of male-defended nesting territories. The hidden lek hypothesis was developed from a study of Razorbills and has been tested with two other species.

My aim here is to summarise the ideas and research that have recently begun to incorporate sexual selection into the study of coloniality. In my original formulation of the hidden lek hypothesis, I stressed extra-pair copulation as the primary source of sexual selection in monogamous species. Here, I consider the possibility that the selection of breeding partners can also cause the lek mechanisms to operate. If this occurs, it may be possible for the lek models to help explain coloniality of monogamous birds even when few or no EPCs are performed. Finally, I will propose general ideas about how sexual selection can be synthesised with mechanisms involving breeding habitat selection, a fusion that we named with the term of ‘ commodity selection’ and that is necessary for building a well balanced framework for studying coloniality (Danchin & Wagner 1997).

In monogamous species, only one female can pair with the highest quality male in an area, but all females can potentially obtain EPCs from him. Monogamy, therefore, sets the stage for sexual selection (Møller 1992). The hidden lek hypothesis assumes that the constraints imposed by monogamy selects for females to preferentially pair with males that provide them with access to better quality males. Such a female strategy could create a simple mechanism that produces nesting aggregations: males that claim territories far from higher quality males may be less able to attract mates, forcing them to readjust their territorial claims and move closer to better males. Although breeding near a higher quality male may cause some males to lose paternity, they would achieve higher fitness by sharing paternity than by foregoing reproduction (Wagner 1993). These circumstances may be produced by the mechanisms of two of the three predominant models of lek formation, the hotshot model (Beehler & Foster 1988) and the female preference model (Bradbury 1981). Although both models were proposed to explain the specific form of aggregation that comprises leks, their mechanisms are extremely general and can be applied to explain male aggregations of many other kinds (Wagner 1997). The hotshot model predicts that leks form when secondary males cluster around a dominant ‘ hotshot’ male who obtains a disproportionate share of matings due to his superior competitive abilities (Beehler & Foster 1988) or his greater attractiveness to females (Hoglund & Roberston 1990). The prevalence of females around the hotshot draws in less attractive males, resulting in the formation of a lek around the top male. The female preference model proposes that males aggregate in response to female preferences for appraising males in groups, where females can make simultaneous comparisons. The model’s mechanism is simply for females to bypass males that display solitarily, forcing them to relocate their display territories next to those of other males. This mechanism may also contribute to colony formation by compelling males to relocate their nesting territories near other males (Wagner 1993).

The hidden lek hypothesis was developed from the mating system of Razorbills, a monogamous, colonial seabird. The species had not previously been known to engage in extra-pair copulation, and their relatively sparse breeding densities appeared to limit the possibility of such social interactions occurring frequently (Birkhead 1978). In the study colony on Skomer Island, Wales, most pairs nested underneath boulders which afforded protection from predators, but limited encounter rates with neighbours. However, Razorbills attended crowded ledges outside the boulder colonies where they aggregated at densities 50 times greater than in the colony (Wagner 1992a), making it possible to record 8000 mating and fighting events in 250 hours of observation (Wagner 1992a, 1992b). These ledges served as mating arenas in which paired males and females engaged in EPCs when their mates were absent, or copulated with their mates when the pair was present. Nearly all females were subjected to EPC attempts in the arenas, and 50% of females accepted one to seven EPCs prior to egg-laying. The discovery of this ‘secondary mating system’ elucidated a number of features of Razorbill behaviour that are applicable to many other monogamous species. The most important finding is that the mating arenas shared all of the features of leks: females visited for copulations with males who did not provide parental care for their offspring (males only provided care for their own offspring and never to those of females with whom they had EPCs (Wagner 1992c)). Males aggregated for these copulations, and as is typical of leks, males fought aggressively over EPCs, timing their fights to coincide with the fertile period of females, and also as in leks there was a male-biased sex ration in the mating arenas.

The conditions in the Razorbill mating arenas bore a striking resemblance to those predicted for lek formation by the hotshot model (Wagner 1992d). As in many leks, there was a marked skew in male dominance, with the top male winning 93 fights compared to a mean of 13, and as predicted by Beehler & Foster (1988), the skew in fighting ability was significantly correlated with a skew in male mating success. In one year, for example, the top fighter obtained 44% of the EPCs, much like males in some lekking species (Pruett-Jones 1988; Hoglund & Alatalo 1995). These findings suggest that the hotshot mechanisms may have produced aggregations of monogamous males.

The mechanism of the female preference model might also help explain the formation of the Razorbill arena (Wagner 1993). If females attain benefits from the aggregation of males then female preferences may select for male attendance in the arenas. This could result if females preferentially visit aggregated males over solitary males (Bradbury 1981; Alatalo et al. 1992).

If the lek mechanisms can cause monogamous males to cluster on a ledge outside of their colony, then they may also cause males to aggregate in locations where colonies subsequently form. All that would be necessary for the Razorbill mating arena to form into a colony would be for Razorbills to remain on the ledge and once paired, lay their eggs there. If Razorbills were to do so, they would be breeding densely on an open ledge, much like many other colonial species. By visiting the mating arenas, where there were no resources other than males, females clearly demonstrated receptivity to extra-pair copulations. Although Razorbills are the only monogamous species known to mate in arenas, the behaviours they perform in the arenas are typical of those performed by other species of monogamous birds within their nesting colonies. The Razorbill arena, therefore, serves as a model for the social behaviours of colonial species, minus the confounding factors associated with nesting-territory defence. The hidden lek hypothesis has been supported by results from studies of two species that are ecologically and phylogenetically distant from Razorbills and each other - Purple Martins and Bearded Tits.

Morton et al. (1990) proposed a causal link between EPC and coloniality based on their findings in Purple Martins, in which males occur in two age classes. One year old males suffered very high frequencies of cuckoldry, losing paternity of most of their broods, whereas older males obtained nearly complete paternity. Old males arrive early from migration, defend nesting cavities, and pair and breed with early arriving (mainly old) females. Old males appear to recruit young males and females to the colony by performing a loud pre-dawn song that coincides with the yearlings’ arrival from migration. Old males then obtain EPCs from the mates of the young males. Thus, the conditions predicted by the hidden lek hypothesis for colony formation (i.e. male aggregation for EPCs, female pairing with males that provide them with access to other males), appear to exist in the Purple Martin colony, with one important exception: the EPCs appeared to be forced (Morton 1987). If females are inseminated forcibly by old males in colonies, then they would be expected to avoid colonies when other breeding sites are available, which is often the case (Morton et al. 1990). Additionally, young males would be selected to avoid breeding near old males. However, as Westneat et al. (1990) proposed and Razorbills illustrate (Wagner 1991), females may resist EPCs as a ploy to test males rather than to avoid insemination. Thus, the question of which sex controls extra-pair copulation is often difficult to resolve (McKinney et al. 1984; Westneat et al., 1990; McKinney & Evarts 1997), and yet is central to the proposed links between sexual selection and colony formation. Wagner et al. (1996a) found strong evidence that female Purple Martins pursue EPCs and are rarely, if ever, forced: females paired to old males almost always avoided EPCs, regardless of the age of the female, the operational sex ratio, and the mate guarding intensity of the male mate. Females paired with young males, however, did accept EPCs. As predicted, we also found that all extra-pair fertilisations were obtained by old males. In both years of the study, a single old male obtained most of the fertilisations, producing a marked skew in male mating success resembling that of leks. These results suggest that the lek mechanisms can create nesting aggregations via EPC and mate choice: young females are attracted to old males for EPCs (when old males are unavailable as mates), while young males are drawn to young females to acquire them as mates.

The Purple Martin study revealed that a colony can possess some key behavioural features of leks. Hoi and Hoi-Leitner (1997) designed a study specifically to test the hidden lek hypothesis in Bearded Tits, which are excellent subjects because females incite extra-pair males, as well as their own mates, to pursue them for copulations (Hoi 1997). Females copulate with the male that outcompetes the other males, thereby maximising the probability of being fertilised by high quality males, a mechanism of sexual selection identified by Cox and Le Boeuf (1977). Females in superior condition (as measured by fat score) initiated flight chases more than females in poor condition, suggesting that they were able to pay the energetic costs of intersexual chases. The high quality females also had the highest frequencies of extra-pair fertilisations and tended to breed in colonies, whereas low quality females and their mates bred solitarily. Confirming their behavioural observations with genetic data, Hoi and Hoi-Leitner found that 43% of colonial females produced extra-pair offspring compared with 0% of solitary females. Furthermore, the authors found no benefits of breeding in higher density: foraging success and predation rates were not significantly different for solitary and colonial breeders. Because of the overt behaviour of females in initiating flight chases, as well as the other evidence, the authors concluded that the pursuit of EPCs by females led to the aggregation of nests of the colonial breeders.

These two studies provide the first evidence that the lek mechanisms may produce nesting aggregations when monogamous species pursue EPCs, providing a promising start to the integration of sexual selection in coloniality research.

In this section I suggest how the hidden lek hypothesis might explain coloniality even in the absence of EPCs. In short, the potential explanation is that the lek mechanisms might operate to produce nesting aggregations when males and females pursue long term strategies for acquiring breeding partners.

As Birkhead & Møller (1996) have noted, many species of monogamous seabirds have low levels of extra-pair paternity. This either means that they perform few extra-pair copulations or that EPCs rarely result in fertilisation because of the paternity assurance tactics of males. If EPC is rare in many colonial species, it raises the question whether the hidden lek hypothesis is applicable to these species. I have previously stressed the importance of EPC in producing skews in male mating success (Wagner 1993; 1997), and indeed it is such skews that invite comparisons between monogamous and lekking species. However, the general issue is whether sexual selection can create nesting aggregations, and sexual selection in monogamous species can also be produced via selection of breeding partners.

In some species, EPCs are performed outside the female fertile period, and such copulations are used for mate appraisal and acquisition (Colwell and Oring 1989; Wagner 1991). No studies have yet addressed the question of whether EPCs that are performed purely for mate appraisal can produce nesting aggregations. To allow for the following speculations, I will assume that if fertilisable EPCs can produce aggregations, that non-fertilisable EPCs can as well. If so, then it is likely that other mate appraisal behaviours that do not involve copulation can also lead to aggregations. The difference between selecting extra-pair mates and breeding partners is that there is typically a marked skew in male EPC success (Wagner 1997), suggesting a skew in male genetic quality. However, it is likely that skews also exist in the quality of males as parents. In many monogamous species, the ability of a male to provision a brood and provide a safe nesting territory may be the most important criteria of female mate choice. Can skews in the quality of breeding partners produce lek-like conditions? I propose that the hotshot model can operate in this context as well: females prefer to pair with males that provide them with access to the top male. In this context, he is the hotshot because he is the best parent, but he can also possess good genes, providing the female with both direct and indirect benefits. In species that are long-lived and breeding-site faithful, females can pursue a long term mating strategy of attempting to ‘ upgrade’ to a better mate in the following breeding attempt. Females can pursue such a strategy by preferentially pairing with males that provide them with access to better males, whom they can attempt to court throughout the breeding season in the chance of acquiring them in the future. Non-fertilisable extra-pair copulation is one easily identifiable means of courtship, however more subtle means may also be used. In particular, by nesting closely to many neighbours, individuals can advertise their quality as parents to prospective mates. The ordinary, non-sexual acts of feeding nestlings, for example, can thus be used as indicators of individual quality (Carlisle & Zahavi 1986; Wagner 1992c; Wagner et al. 1996b; Freeman-Gallant 1997; Zahavi & Zahavi 1997; Lotem et al. in press). Even in long-lived, mate-faithful species, divorce and mortality can produce considerable opportunity for re-pairing (Coulson and Thomas 1983), permitting a long term mate acquisition strategy. If females do prefer to breed near high quality mates that are already paired, it could cause other males to claim territories around top males. Thus, even without extra-pair copulation, the lek mechanisms might produce nesting aggregations.

The above scenario assumes that females, by being choosy in mate choice, strongly influence male settlement decisions. However, when males contribute parentally, they are also selective in mate choice (Trivers 1972). This raises the question of whether the lek mechanisms can also operate when males are selective. A promising line of investigation, therefore, will be to determine whether males prefer to breed near males who provide them with access to better females.

Until now, I have focused exclusively on sexual selection as an overlooked mechanism of colony formation. However, in order to build an integrated approach to studying coloniality, it is necessary to synthesise sexual selection and natural selection (Danchin & Wagner 1997). A new natural selection-based hypothesis by Boulinier & Danchin (1997) and Danchin et al. (1998) allows for the start of such a synthesis. The ‘ habitat selection’ hypothesis (Boulinier & Danchin 1997; Danchin et al. 1998) is built upon ideas about conspecific attraction, the widespread phenomenon of animals being drawn to members of their species (reviewed in Danchin & Wagner 1997). Selection of breeding habitat based on conspecific cues has long been recognised as a general mechanism of aggregation (Shields et al. 1988; Stamps 1988; Reed & Dobson 1993; Forbes & Kaiser 1994; Muller et al. 1997). Individuals can exploit conspecifics by gaining ‘ public information’ from them, providing a mechanism of aggregation that has been well documented (Valone 1989, 1996, Valone and Benkman this symposium). The findings of Danchin et al. (1998) add a critical dimension to previous work on conspecific attraction, namely that animals choose breeding sites not only when they are occupied by conspecifics, but when they are occupied by conspecifics with high reproductive success. This finding was made in their long term study of Kittiwakes Rissa tridactyla. In the study population there is high variance in RS among 45 cliffs between years, which is often produced by heavy predation or parasitism on some cliffs, and little or no predation nor parasitism on others (Danchin et al. 1998). In selecting breeding habitat, Kittiwakes either return to the same cliff as in the previous year, or disperse to a new cliff. Danchin et al. (1998) found that the habitat selection strategy of Kittiwakes is to return to the same cliff when successful, but when unsuccessful, their decision depends upon the RS of other Kittiwakes on the same cliff. When their nesting neighbours have low RS, they disperse. But when most or all neighbours are successful, failed breeders return to the same cliff. This indicates that public information on the RS of conspecifics over-rides individual experience. Breeders from failed cliffs and young pre-breeders gather information about habitat quality by visiting other cliffs where they observe the reproductive performance of conspecifics (Cadiou et al. 1994). Such end-of-season prospecting for future breeding sites is prevalent in many species (Coulson & Porter 1985; Reed & Oring 1992; Reed & Dobson 1993; Cadiou et al. 1994; Boulinier et al. 1996; Reed et al. in press). As suggested by Boulinier et al.’s experiment (this symposium), the presence of chicks in the nests or the social activities of chick rearing seems to constitute a key cue attracting potential prospectors.

Why don’t all breeders crowd onto the same high quality cliff and simply return each year? The answer is that the system is dynamic: cliff quality (as measured by mean RS) varies between years. It is fairly predictable from year 1 to year 2 but the auto-correlation fades thereafter and breaks down completely by year 4 (Danchin et al. 1998). Prospectors obtain higher fitness by recruiting to recently successful cliffs than by randomly selecting breeding habitat (Boulinier & Danchin 1997). Thus, there is strong continuous pressure for first time breeders and breeders from failed cliffs to prospect for habitat for the following year. During the peak of breeding, conspecifics provide a maximum amount of public information - some nests are filled with healthy chicks while other cliffs hold predated nests. Individuals can benefit by breeding as closely as possible to successful conspecifics in order to experience the same favourable conditions. This simple mechanism can produce aggregations and play an important role in the evolution of coloniality (Danchin et al. 1998). The habitat selection hypothesis is elegant because it provides the elusive common currency for such diffuse breeding requirements as food availability, safety from predators and low ectoparasite infestations. Individuals are not required to evaluate a complex matrix of environmental factors that determine habitat quality. Instead, they can parsimoniously base their decision upon a single cue: conspecific reproductive success.

Evidence now exists that sexual selection and habitat selection contribute to colony formation. Thus far, however, each process has only been studied independently. In this section I will suggest, briefly, how these two processes might interact. The interaction of mate choice and habitat selection clearly occurs in many species, because mates and habitat are often selected simultaneously, especially by females who often select males with established territories, as in Kittiwakes (Fairweather & Coulson 1995). Some of the work summarised here has shown that the lek mechanisms can operate in contexts much more general than those in which they were originally proposed. In addition to contexts involving sexual selection, the lek mechanism may even operate in conjunction with habitat selection. This occurs if, as in the Kittiwake system, prospectors concentrate on cliffs with high RS not only because of good breeding conditions, but also because of the probability of finding high quality mates there. In this way, conspecific attraction could produce aggregations of males and females seeking both good breeding habitat and good mates.

Another potential intersection of mate and habitat selection involves the fact that many species prospect for breeding territories at the end of the breeding season (Reed et al. in press). This is intriguing, because end-of-season ‘ prospecting’ for mates is also known (Coulson & Thomas 1983; Wagner 1991), although it has not yet been rigorously studied. In Razorbills, females remained in the colony while their mates escorted the fledgling to sea. At this time, females consorted and often copulated with extra-pair males. Females and extra-pair males also performed standard courtship behaviour such as ‘ billing’ and allopreening (Bedard 1969) that suggest that not only copulation, but also other sexual behaviour, may lead to new pair bonds. One such post-season consortship did lead to a new pair-bond in the following year. A promising line of research will be to study the behaviour of individuals at the end of the breeding season as they visit prospective breeding sites and consort with prospective mates.

Evidence has begun to accumulate that the processes of mate choice can contribute to colony formation. Boulinier & Danchin (1997) and Danchin et al. (1998) have shown that breeding habitat selection can also produce mechanisms of nesting aggregations. By studying sexual selection and habitat selection in tandem, we can identify general mechanisms that produce breeding aggregations (Danchin & Wagner 1997). This approach combines the ultimate factors that determine fitness with the proximate mechanisms that may produce colonies; variation in the quality of prospective mates and in the RS of conspecifics provides proximate cues that breeders use to optimise their fitness. Together, the hidden lek and habitat selection hypotheses involve the assessment and selection of all the commodities necessary for reproduction: food, safety from predators, avoidance of parasites, mates, fertilisations and breeding sites etc. Thus ‘ commodity selection’ may be the common thread of coloniality (Danchin & Wagner 1997).

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