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Introduction

Extrapair paternity (EPP) provides socially monogamous males the opportunity to increase their reproductive success by siring offspring outside of their pair bonds, usually without the cost of parental care. Although the advantages of EPP for extrapair sires are clear, most current adaptive hypotheses for EPP in birds have emphasized the benefits of EPP for females (henceforth the “female benefits” hypotheses; reviewed in Griffith et al. 2002; Akcay and Roughgarden 2007; Kempenaers 2007; Mays et al. 2008). The idea that EPP is part of mixed reproductive strategy driven by females arose because behavioral evidence suggests that females solicit extrapair fertilizations in some taxa (reviewed in Westneat and Stewart 2003), males without intromittent organs might be unable to fertilize unwilling females (Gowaty and Buschhaus 1998), and females are generally the choosier sex (Trivers 1972).

The most frequently invoked female benefits hypotheses are the good genes, genetic compatibility, genetic diversity, and direct benefits hypotheses (reviewed in Griffith et al. 2002; Cockburn 2004). According to the good genes and genetic compatibility hypotheses, females select extrapair sires that are either of higher genetic quality than their within‐pair males or that are more compatible with themselves than they are with their within‐pair males, thereby producing extrapair young (EPY) of higher quality than their within‐pair young (WPY). The genetic diversity hypothesis suggests that females seek fertilizations from multiple sires in order to produce, by chance, offspring suited to a wide variety of environmental conditions. Finally, the direct benefits hypothesis suggests that females seek a resource from extrapair sires in exchange for their paternity. Most previous studies have focused on a single female benefits hypothesis, even though females might gain one benefit but not another (Bouwman et al. 2006), multiple benefits from a single sire (Fossoy et al. 2008), or different benefits from different extrapair sires (Rubenstein 2007).

Recently, a number of models, meta‐analyses, and reviews have questioned whether EPP is driven primarily by the interests of male or female birds. In their review, Westneat and Stewart (2003) pointed out that extrapair copulatory behavior is rarely documented and, when observed, does not always appear to be initiated by females. Arnqvist and Kirkpatrick (2005) suggested that females accept extrapair fertilizations to alleviate harassment by extrapair males, rather than for potential benefits of EPP, because punishment by within‐pair males generally outweighs genetic benefits gained by females (but see Arnqvist and Kirkpatrick 2007; Griffith 2007). Examining the same data set, however, Eliassen and Kokko (2008) concluded that available information is insufficient to assess whether EPP is generally male or female driven. Across species, meta‐analyses and reviews have yielded mixed evidence for the good genes and genetic compatibility hypotheses (Akcay and Roughgarden 2007; Kempenaers 2007; Mays et al. 2008), leading some authors to suggest that these hypotheses lack general support (Akcay and Roughgarden 2007; Mays et al. 2008).

In this study, we use multiple broods from long‐lived, socially monogamous American crows (Corvus brachyrhynchos) to simultaneously test four of the female benefits hypotheses, comparing the predictions of these hypotheses to what we would predict if EPP was primarily male driven in this system. American crows in this population breed in cooperative family groups that include a socially monogamous pair, assisted at the nest by 0–10 auxiliaries of either sex (2004–2007 birds; Townsend, forthcoming). Although auxiliaries are often offspring from previous broods, some auxiliaries are stepsons of the female breeder, nondescendant kin of the male breeder, or completely unrelated birds (Townsend et al. 2009b). American crows are an excellent system in which to test the female benefits hypotheses because direct benefits of EPP, which are difficult to define or measure in most taxa (Akcay and Roughgarden 2007), can be clearly defined as parental care provided by within‐group extrapair sires (Cockburn 2004). Furthermore, the assumption that females are more compatible with less related males, which has been made by most tests of the genetic compatibility hypothesis (Akcay and Roughgarden 2007; but see Shields 1982; Tregenza and Wedell 2000), appears valid in this system: highly inbred offspring in this population have a relatively low survival probability (Townsend et al. 2009a). Another strength of this study system is that the frequency of observed extrapair copulation (EPC) attempts involving a given female predicts the proportion of EPY she produces (Townsend, forthcoming), suggesting that patterns of genetic paternity can be used to infer patterns of female copulatory behavior in this population (Griffith 2007).

We examined American crow paternity in relation to offspring condition, inbreeding and survival, and parental relatedness and provisioning efforts. We predicted that if females chose extrapair sires of higher genetic quality or compatibility than their within‐pair sires, then EPY would be in better condition and have a higher survival probability than WPY within individual broods. If the genetic benefits of EPP were gained from parental compatibility, then we predicted that EPY would be less inbred than WPY within these broods; similarly, we predicted that the proportion of EPY would increase with the relatedness of the social pair. If females engaged in EPC because they derive benefits from genetic diversity among their offspring, then we predicted that genetically diverse broods would generate more surviving offspring than less diverse broods and that most or all females would engage in EPP (Bouwman et al. 2006). If females engaged in EPC to gain direct benefits from extrapair sires, then we predicted that provisioning rate would be higher in broods belonging to groups containing within‐group extrapair sires, or female breeders in groups with within‐group extrapair sires would themselves benefit by reducing their own provisioning efforts. Furthermore, we predicted that increased provisioning (or other forms of parental care provided by extrapair sires, such as sentinel behavior and nest defense; Wilson 2008) would lead to increased survival of all offspring in broods produced by groups containing within‐group extrapair sires. The female benefits hypotheses and selected predictions are summarized in table 1.

Table 1: Summarized predictions of four hypotheses proposing that females benefit from extrapair paternity (EPP), compared with predictions if EPP was generally male driven

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We compared these predictions of the four female benefits hypotheses to what we expected if EPP was generally male driven in American crows. Under the male‐driven scenario, females would not necessarily derive any benefits, either genetic or direct, from extragroup males. However, some predictions of the direct benefits hypothesis (e.g., increased brood provisioning rate in groups containing within‐group extrapair sires, along with increased offspring survival) were the same as what we expected if EPP was male driven: within‐group extrapair sires might invest more effort in the care of broods in which they have sired offspring, regardless of the interests of the female breeder.

Methods

Results

Of 283 offspring from 83 broods belonging to 26 family groups, 234 were produced by within‐pair sires (82.7%), 26 were produced by extragroup extrapair sires (9.2%), and 23 were produced by within‐group extrapair sires (8.1%). Ten offspring sired by within‐group extrapair sires were produced from mother‐son matings. Fifteen of 29 female breeders (52%) did not have EPY in any of their broods. Among 26 fully genotyped social pairs, KINGROUP identified five pairs (19.2%) that were likely to be second‐order kin. No socially monogamous pairs were likely first‐order kin. Parentage did not affect nestling size (LME with parentage, age, year, and sex as fixed effects and social pair as a random effect; , ) or nestling mass, with or without statistically accounting for size (LME with parentage, size, size × size, year, and sex as fixed effects and social pair as a random effect; , and LME with parentage, year, sex, and age as fixed effects and social pair as a random effect; , ). Likewise, mark‐recapture analysis indicated no strong paternity effects on apparent survival or recapture probability: a fully time‐dependent model without paternity effects was most strongly supported by the data ( ; table A1). Although we have shown elsewhere that highly inbred offspring have a lower survival probability than relatively outbred offspring (Townsend et al. 2009a), there were too few incestuously produced EPY ( ) in this sample to analyze them separately from other EPY.

Offspring inbreeding index (IR) varied with paternity (LME with social pair as a random effect; , ): offspring sired by within‐group extrapair sires were more inbred than WPY (Tukey’s HSD, ; fig. 1). When we removed the 10 offspring produced by matings between mothers and adult auxiliary sons from the model, inbreeding index did not vary with paternity (LME with social pair as a random effect; , ). The parental relatedness coefficient did not explain the proportion of EPY for a given parental pair, either when the proportion of all extrapair young (GLM; , , ) or the proportion of extragroup extrapair young (GLM; , , ) were considered as the response.

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Figure 1: Mean inbreeding index ± SE of offspring produced by within‐pair sires, extragroup extrapair sires, and within‐group extrapair sires.

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We conducted 99 nest watches on 30 broods from 20 family groups in 2007 and 2008. Mean provisioning rates for male and female breeders, all auxiliaries combined, and for all group members together were , , , and visits/h, respectively. After accounting for number of auxiliaries in the group, auxiliary and overall provisioning rates were higher at broods with potential within‐group extrapair sires (table 2). Although we could not quantify individual auxiliary provisioning rates in this study, the increased provisioning rate in groups with multiple potential within‐group sires did appear to be driven by a markedly high provisioning rate by potential within‐group extrapair sires (A. K. Townsend, personal observation). The provisioning rate of male and female breeders did not change when multiple potential within‐group sires were present (table 2), suggesting that cuckolded males did not punish their females and that extrapair sires did not lighten breeder workload.

Table 2: Provisioning rates (visits/h) and presence of potential within‐group extrapair siresa

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Broods with potential within‐group extrapair sires produced more nestlings (GLMM with social pair as a random effect; when potential within‐group sires present vs. absent , , ) and more fledglings (GLMM with social pair as a random effect and year as a fixed effect; when potential within‐group sires present vs. absent , , ). When 13 depredated broods were included in the sample, multiple within‐group sires had no significant effect on number of surviving offspring at any stage (data not shown). Presence of offspring sired by extragroup extrapair sires had no detectable effect on brood output (table A2).

Discussion

In our population of American crows, females derived no apparent benefits from extragroup extrapair sires. Counter to the predictions of the good genes and genetic compatibility hypotheses, EPY were not in better condition, heavier in mass, larger in size, or less inbred than WPY, nor did they have a higher survival probability than WPY, and the frequency of cuckoldry did not increase with the relatedness of the social pair. Counter to the predictions of the genetic diversity hypothesis, most females did not engage in EPP, and brood output was not higher from diverse broods. From within‐group extrapair sires, however, females appeared to both suffer costs and gain benefits. Ten offspring produced by within‐group extrapair sires (constituting 4% of all sampled offspring) resulted from matings between mothers and their adult auxiliary sons, leading to higher mean inbreeding indices for within‐group EPY than for WPY. Previously in this population, we showed that offspring with high inbreeding indices have a lower probability of survival than relatively outbred birds (Townsend et al. 2009a). In this study, however, any reduction in survival probability of incestuously produced EPY appeared to have been outweighed at the brood level by the direct benefits provided by within‐group extrapair sires. There was a higher number of surviving offspring in groups containing multiple potential within‐group sires, which might have been due, in part, to the higher auxiliary provisioning rate in these groups.

There are at least two interpretations of our results. First, females might choose to engage in EPCs for the direct benefits they gain from within‐group extrapair sires, and for some unmeasured benefit gained from extragroup extrapair sires. They might, for example, choose to mate with extragroup males for fertility insurance (Griffith et al. 2002), to gain superior alleles for a trait that we did not measure (e.g., competitiveness; Kempenaers 2007) or for an additional direct benefit (e.g., territory access; Gray 1997).

The second interpretation is that EPP is primarily a male‐driven strategy that is variously costly, beneficial, and neutral for female American crows. Females did not appear to derive any of our hypothesized benefits from fertilizations by extragroup extrapair sires. The direct benefits that they accrued from potential within‐group extrapair sires might have been incidental to the interests of extrapair sires themselves, who had a personal fitness interest in maximizing the survival probability of their own offspring, in addition to their interest in the success of their nondescendant kin in the brood. The male‐driven interpretation is supported by behavioral observations of EPCs in American crows (Kilham 1984; Townsend et al. 2009b): female crows appear to resist EPC attempts by extrapair males from both within and outside of their groups. Some of the males observed attempting to force EPCs ultimately succeed in siring offspring with these females (Townsend, forthcoming), consistent with the idea that females might sometimes accept unwanted EPCs to reduce the costs of harassment (Westneat and Stewart 2003; Arnqvist and Kirkpatrick 2005). Eliassen and Kokko (2008) suggested that females should accept unwanted EPCs when the costs of resisting them exceed the costs of accepting them. In crows, accepting EPCs did not appear to lead to a reduction in male parental care, the most widely proposed cost (e.g., Eliassen and Kokko 2008), although accepting EPCs might have entailed other costs (e.g., inbreeding depression).

This study has added to other studies suggesting that breeding females gain extra help from extrapair males in cooperatively breeding birds (Li and Brown 2002; Rubenstein 2007; but see Williams and Hale 2008). We note, however, that correlations between EPP and the direct benefits that we observed were not necessarily causal. It is possible, for example, that auxiliary males that are relatively good providers are also those that are more likely to attempt EPCs. Furthermore, even if EPP does lead to direct benefits in cooperative systems, these results might not be widely applicable to noncooperative systems. Despite the fact that the direct benefits hypothesis is among the leading hypotheses set forth to explain the occurrence of EPP in birds, the forms that direct benefits might take in noncooperative species are less clear (although see Gray 1997).

In cooperatively breeding species, individuals sometimes interact with related adults of the opposite sex, and the opportunity for inbreeding is therefore relatively high (Alexander 1974). In this crow population, we observed occasional mother‐son incest, and 19% of social pairs appeared to be second‐order kin. Inbreeding depression has been hypothesized as a driving force behind sex‐biased dispersal in many taxa (Charlesworth and Charlesworth 1987), and the regular occurrence of inbreeding in this large, open population of crows with severe inbreeding depression begs explanation (Townsend et al. 2009a). In the case of the mother‐son incest, the cost of lower survival probability of the most inbred individual offspring might have been outweighed, at the brood level, by increased parental efforts by the auxiliary sires. Kin selection might also play a role in the occurrence of inbreeding in this population: a female breeding with a related pair male or auxiliary son is improving the mating success of a relative, thereby increasing her own inclusive fitness (Kokko and Ots 2006), as long as some of these offspring survive. Inbreeding costs might be further defrayed if inbreeding enhances within‐group cooperation (Alexander 1974) or maintains locally selected gene complexes (Shields 1982).

Most recent examinations of variation in EPP have focused solely on the idea that breeding females drive the occurrence of EPP among individuals within a population. Across species, however, support for the female benefits hypotheses has been limited and mixed (Akcay and Roughgarden 2007; Mays et al. 2008), and some authors have proposed that EPP might be primarily male driven (Arnqvist and Kirkpatrick 2005). In this population of American crows, the patterns of parental behavior and offspring characteristics that we observed could be interpreted as consistent with either male‐ or female‐driven EPP. We suggest that neither sex was solely responsible for driving the observed patterns of EPP in American crows. Rather, extrapair fertilizations were likely to reflect the dynamic conflicting or coinciding interests among the within‐pair and extrapair males, as well as the female breeders (see Westneat and Stewart 2003). We suggest that, by considering the interests of all of these involved players, we would have a better understanding of the distribution of EPP among individuals within this population.