Extrapair paternity and mate choice.

Extrapair paternity is now widely recognized as a frequently occurring phenomenon among socially monogamous birds (e.g. Griffith et al. 2002). The extent of extrapair paternity in a population depends on interactions among three individuals: the extrapair male and his ability to obtain extrapair copulations, the social male and his ability to protect paternity in his nest, and the female and her proclivity for seeking extrapair copulations (Westneat et al. 1990, Dunn et al. 1994a). Extrapair paternity appears to be more common in Tree Swallows than in most other species; 50–90% (Dunn et al. 1994a) compared to an average of 14% for other species (Birkhead and Møller 1992), a high frequency that is not an artifact of nest boxes (Barber et al. 1996). In addition, the prevalence of extrapair paternity also varies widely between years within a breeding population (e.g. 50% of broods in one year, 87% the next) and between individuals within a single population (Dunn et al. 1994a). Those factors, when combined with the ability to capture and sample complete family groups, have allowed Tree Swallow researchers a unique opportunity to examine the relative strengths of the three players in the extrapair mating game.

Perhaps the most interesting finding of Tree Swallow extrapair research is that extrapair copulations are almost completely under the control of the female (Venier and Robertson 1991, Lifjeld and Robertson 1992, Venier et al. 1993, Dunn et al. 1994b). In fact, female preference appears to override most other factors that have the potential to influence the opportunity for extrapair activity (e.g. nest-box location, nest-box density, breeding synchrony, experience; Dunn et al. 1994b). However, there are no consistent across-year patterns with respect to the characteristics of males selected by females (e.g. size, experience, arrival date) that allow the clear definition of a high-quality mate (Dunn et al. 1994a, Barber et al. 1998, Conrad et al. 2001). Indeed, one could conclude from those studies that the definition of a high-quality mate is not a fixed definition; rather, it may change both with and among breeding seasons as ambient conditions change (e.g. weather, food availability, talent pool).

Importance and role of floaters

Whenever breeding resources are limited, there is a potential for a proportion of a population to be unable to breed despite being reproductively mature (e.g. Brown 1969, Smith 1978). In some species, such as the Tree Swallow, that proportion can be quite large (Stutchbury and Robertson 1985). As a consequence, understanding the role of floaters can be an important component of understanding a species’ population dynamics.

There are at least three theories concerning the characteristics of floating individuals. The first theory contends that floating individuals are younger or competitively inferior individuals or both who were unable to obtain a breeding opportunity (e.g. Shutler and Weatherhead 1992). The second theory contends that individuals choose to forego breeding in the hope of obtaining a high-quality nest site or territory should one come available (e.g. Zack and Stutchbury 1992). The third theory contends that floating is a viable alternative reproductive strategy to holding and defending a nest-site or breeding territory. For females, that could take the form of intraspecific brood parasitism (Gowaty 1985, Sandell and Diemer 1999); for males, extrapair paternity (Petrie and Kempenaers 1998).

Tree Swallows, as secondary cavity nesters, are often strongly nest-site limited (Holroyd 1975). As a consequence, there are always individuals of both sexes who are unable obtain to nest sites or mates or both. Female Tree Swallows do not reproduce until they can obtain a nest site (Stutchbury and Robertson 1987b); intraspecific brood parasitism is very uncommon in this species (Lombardo 1988, Barber et al. 1996, Kempenaers et al. 1999). Most female floaters are one-year-old females (Stutchbury and Robertson 1987b) who do not breed although they do spend a considerable amount of time prospecting for nest sites.

The Tree Swallow is one of only two species in North America in which only the female and not the male displays delayed plumage maturation (Hussell 1983, Stutchbury and Robertson 1987a; the other is the Hooded Warbler [Wilsonia citrina], Morton 1989). Subadult Tree Swallow females have a dull brownish plumage that contrasts strongly with iridescent blue plumage of adult males and females (Hussell 1983). Stutchbury and Robertson (1987a) hypothesized that the distinctive plumage of subadult females served to reduce aggression by resident males (sexual signaling) and resident female (subordinate signaling), thereby facilitating exploration. Resident males tended to be less aggressive to subadult females than to intruding adult females, whereas resident females were equally aggressive towards subadult and adult intruders. Those results and others (Lozano and Handford 1995) imply that female subadult plumage is primarily an intersexual signaling adaptation.

Unlike female floaters, however, male floaters are able to obtain a modest degree of reproductive success despite not defending a nest box. In one study (Kempenaers et al. 2001), floaters were responsible for 13% of extrapair young to which the researchers could assign paternity. Again unlike females, there were few differences—morphological or otherwise—between floater and resident males, other than a tendency for males who participated in extrapair matings (including floaters) to be heavier than those that did not. That study supported previous observations that male floaters participate in extrapair copulations (Barber and Robertson 1999), but was one of the first to document successful reproduction by floaters in any passerine species (see Ewen et al. 1999).

Mate guarding, paternity confidence, paternal care, and infanticide

Ever since researchers confirmed the existence of extrapair mating strategies in birds, there has been an interest in (1) whether or not males can prevent females from engaging in extrapair activity and vice versa, and (2) whether or not males can tell if there are extrapair young in their own nests. Male birds employ several behaviors in an attempt to minimize the extrapair activity undertaken by their social mate. First, they can attempt to prevent the settlement of conspecific pairs nearby (Rendell and Robertson 1994). Second, they can maintain visual vigilance over their social mate and interrupt any extrapair activity (Birkhead 1979). Third, males may attempt to copulate with their social mate as frequently as possible to win the sperm competition battle (Birkhead et al. 1989). Research into those behaviors in Tree Swallows has led to the conclusion that male behavior is largely dictated by female activity (Chek and Robertson 1994, Whittingham et al. 1994). Given that female Tree Swallows appear determined to participate in extrapair activity, frequent copulation may be a more efficient strategy to insure paternity than is intense following (Venier and Robertson 1991, Whittingham et al. 1994); it is less energetically costly and provides the male opportunities to pursue his own extrapair activities. However, given the prevalence of extrapair young in Tree Swallow nests (Lifjeld et al. 1993), it appears that whatever strategy males adopt are not particularly effective. Indeed, mate guarding (either by following or frequent copulation) may only be a viable paternity confidence strategy when females have little interest in pursuing extrapair activities (Chek and Robertson 1994).

How males ascertain the presence of extra-pair young in their nests is unclear. Because it is difficult to test nestling recognition by males directly in the field, we need to identify behaviors that are proxies for paternity confidence. One obvious candidate is male parental care. Building on parental-investment theory which predicts a decrease in male parental care with a decrease in paternity confidence (Trivers 1972), Whittingham et al. (1992) outlined a theoretical framework for the trade-offs among paternity

confidence, male parental care, and offspring recruitment. In species such as the Tree Swallow, where male care positively affects offspring recruitment (Leffelaar and Robertson 1986), one would predict a positive relationship between paternity confidence and male parental care; the shape of the curve depends on the strength of the relationships between care and recruitment. In Tree Swallows, empirical evidence indicates that paternity confidence appears to have little effect on male parental care unless the probability of paternity is very low (Robertson 1990, Whittingham et al. 1993); that matches findings for other socially monogamous species (e.g. Indigo Bunting [Passerina cyanea]; Westneat 1988). There are at least two reasons for that lack of a relationship. One is that males are unable to assess the proportion or likelihood of extrapair young in their nests, except in extreme cases. If that is the case, then it behooves males to continue caring for nestlings on the chance that some of them are theirs. Alternatively, males may feel “confident” in their guarding behaviors such that they have no need to question the paternity of their brood. Females may bolster that confidence by soliciting and accepting copulations from their social mates after absences from the nest site (Kempenaers et al. 1998).

Another alternative avenue to examine a male’s ability to assess paternity is to perform a removal experiment (i.e. remove the resident male) and monitor the behavior of the replacement male. Removal experiments with Tree Swallows have led to some interesting and startling results concerning the lengths that males will go to insure paternity (Robertson and Stutchbury 1988, Robertson 1990). If a male is removed during the egg-laying stage, the replacement male tends to adopt the brood, because there is a probability that he has at least partial paternity (Robertson 1990). Replacement males that arrive after clutch completion but early in incubation tend to adopt the brood whereas males that arrive late in incubation tend to commit infanticide, killing the nestlings after they hatch to induce the female to renest. Similarly, replacement males that arrive during the nestling stage almost always commit infanticide (Robertson and Stutchbury 1988, Robertson 1990). Infanticide in Tree Swallows appears to be a sexually selected behavior. Unmated males that are infanticidal are able to obtain a breeding opportunity and, hence, will have a higher potential fitness than unmated males that are not infanticidal (Robertson and Stutchbury 1988, Robertson 1990).

Females are not passive by-standers in that somewhat macabre scenario. Females tend to be receptive to replacement males during egg-laying and incubation and may attempt to pacify the replacement males by readily accepting copulations (Robertson 1991). However, when the replacement male arrives during the nestling stage, females react very aggressively to their presence and may, in some cases, be able to prevent infanticide (Robertson 1991). Interestingly, female Tree Swallows are also known to commit sexually selected infanticide, likely driven by nest-site limitation (Shelley 1934, Robertson and Stutchbury 1988, Chek and Robertson 1991). Chek and Robertson (1991) removed four females during incubation and four during the nestling stage. All the incubation replacements buried the existing eggs with a new nest and laid their own clutch. Only two of the four experimental nestling-removal boxes received a replacement female. One of those females ignored the nestlings until they died; the dead nestlings disappeared from the nest box and she started her own clutch. The second replacement female committed infanticide.