Molecular Ecology (2010) 19, 2328–2335 doi: 10.1111/j.1365-294X.2010.04640.x

Fitness benefits of polyandry for experienced females

L. A. WHITTINGHAM and P. O. DUNN Department of Biological Sciences, University of Wisconsin—Milwaukee, PO Box 413, Milwaukee, WI 53211, USA

Abstract Females often mate with several different males, which may promote competition and increase offspring viability. However, the potential benefits of polyandry remain controversial, particularly in where recent reviews have suggested that females gain few genetic benefits from extra-pair mating. In tree swallows (Tachycineta bicolor), we found that females with prior breeding experience had more sires per brood when paired to genetically similar social mates, and, among experienced females, broods with more sires had higher hatching success. Individual females breeding in two consecutive years also produced broods with more sires when they were more genetically similar to their mate. Thus, experienced females were able to avoid the costs of mating with a genetically similar social mate and realize fitness benefits from mating with a relatively large number of males. This is one of the first studies to show that female breeding experience influences polyandry and female fitness in a natural population of vertebrates. Our results suggest that the benefits of polyandry may only be clear when considering both the number of mates females acquire and their ability to modify the outcome of .

Keywords: breeding experience, extra-pair mating, genetic benefits, genetic similarity, polyandry Received 7 January 2010; revision received 17 March 2010; accepted 25 March 2010

nations of maternal and paternal alleles (Kempenaers Introduction 2007; Puurtinen et al. 2009). Polyandry is a common reproductive tactic in many Social , the most common animals and identifying the factors that influence this in birds, imposes constraints on the availability of social behaviour is important for understanding sexual selec- partners. This may lead to mated pairs that are geneti- tion, yet the adaptive significance of polyandry remains cally similar (i.e. less compatible), resulting in negative elusive (Jennions & Petrie 2000; Griffith et al. 2002; Sim- fitness consequences which can be severe, including mons 2005). For males, there are obvious benefits from reduced hatching success (Bensch et al. 1994; Kempena- mating with multiple females, such as a greater number ers et al. 1996; Cordero et al. 2004; Mulard et al. 2009) of offspring, but the benefits of mating with multiple and lower recruitment (Keller et al. 2002; Kruuk et al. males are less straightforward for females, especially 2002; Szulkin et al. 2007). However, in many species of when females do not gain any direct benefits from birds females play an active role in extra-pair mating males, such as nuptial gifts (Griffith & Immler 2009). It (reviewed in Westneat & Stewart 2003; Pedersen et al. is often suggested that by mating with multiple males, 2006), resulting in genetic polyandry, which can circum- females will increase the likelihood that their offspring vent the constraints of social monogamy and allow gain genes from males that increase offspring fitness. females to gain genetic benefits for their offspring. In The nature of these genetic benefits is unclear, but they particular, attention has focused on the hypothesis that could act through additive (good genes) or non-additive females choose extra-pair males that are genetically dis- (compatible genes) effects that reflect beneficial combi- similar to increase offspring heterozygosity or reduce depression (Fromhage et al. 2009). This Correspondence: Linda A. Whittingham, Fax: +414 229 3926; hypothesis predicts that socially monogamous females E-mail: [email protected] paired to genetically similar males will be more likely

2010 Blackwell Publishing Ltd BREEDING EXPERIENCE AND POLYANDRY 2329 to mate with extra-pair males that are more genetically Materials and methods dissimilar and this will result in greater offspring viabil- ity. Study area and species While several studies of birds have examined this pre- diction (Kempaenaers et al. 1996; Krokene & Lifjeld 2000; We examined genetic similarity of social mates in rela- Keller et al. 2002; Foerster et al. 2003; Hansson et al. 2004; tion to extra-pair mating in unmanipulated broods of Schmoll et al. 2005; Edly-Wright et al. 2007; Stapleton et al. tree swallows over 4 years (1999–2002). Tree swallows 2007; Suter et al. 2007; Fossøy et al. 2008), relatively few are small (20 g), socially monogamous, single- have found that genetic similarity between social mates brooded, migratory passerines that nest secondarily in was associated with the presence of extra-pair young (Ei- tree cavities, but readily breed in nest boxes (Robertson mes et al. 2005; Tarvin et al. 2005; Freeman-Gallant et al. et al. 1992). There are typically four to six eggs per 2006), and none of these have shown that extra-pair mat- clutch which are incubated solely by the female. Our ing increased offspring viability. However, these studies study of tree swallows began at the UWM Field Station have not examined the number of different sires in a near Saukville, Wisconsin (4323¢ N, 8801¢ W) in 1997 brood, which may be a more appropriate measure of and includes 6 ha of fields that have 88 nest boxes, multiple mating than the percentage of extra-pair young, located in two grids 600 m apart. Within grids, nest if females are attempting to diversity the genotypes of boxes are 40 m apart along a row and 28 m apart on their offspring. Furthermore, we might expect females the diagonal between rows, similar to natural tree swal- with prior breeding experience to be better able to find low densities (Robertson & Rendell 1990). Breeding is and gain fertilizations from suitable extra-pair mates. synchronous with 84% of clutches started during the This experience effect could be produced by a variety of last 3 weeks of May (1999–2002) and the level of extra- mechanisms including the ability to modify sperm com- pair paternity is not related to density or synchrony petition after , as well as more traditional pre- (Dunn et al. 1994). copulatory mechanisms, such as the ability to escape the Adults were caught inside nest boxes, weighed, mea- paternity guards of males, assess male traits that indicate sured and marked with a USFWS band on the right leg quality or travel greater distances to sample more poten- and a coloured plastic band on the left leg. Adult sex tial extra-pair mates. To date, however, little is known was determined by the presence of a brood patch or about how breeding experience influences the ability of cloacal protuberance. Unlike many other species, females to assess extra-pair males or gain extra-pair mat- female tree swallows (but not males) show delayed ings. plumage maturation: females are brown in their second We examined the influence of female breeding experi- year (SY) and only possess the blue-green plumage sim- ence and genetic similarity to her social mate on the ilar to males when they are older (ASY; Hussell 1983). number of sires per brood, the genetic dissimilarity of In our analyses, age was coded as SY or ASY. In this the female to her extra-pair mate(s), and the impact of study, 88% of females were blue-green ASY females. sire diversity on offspring hatching success in the We also examined the effect of prior breeding experi- socially monogamous tree swallow (Tachycineta bicolor), ence in our population. Females were considered expe- a small passerine bird. Tree swallows have one of the rienced breeders if they had bred in a previous year in highest reported levels of both extra-pair paternity our population, and inexperienced breeders if they (50% of young and 88% of broods) and multiple pater- were new to our population (i.e. unbanded; Robertson nity in birds (most broods contain three to six different & Rendell 2001). Tree swallows have an average life- sires; Whittingham et al. 2006; Dunn et al. 2009). span of only 2.7 years and usually breed only 1–2 years Behavioural and experimental evidence suggest that (Robertson et al. 1992), thus, most of our ASY females female tree swallows pursue extra-pair matings, and were probably 2 or 3 years old. they have significant ability to control which males fer- We checked nest boxes daily to determine laydate, tilize their eggs (reviewed in Whittingham et al. 2006; clutch size, hatching success and fledging success. Nes- Dunn et al. 2009). Furthermore, mean heterozygosity of tlings were weighed and measured (tarsus and ninth broods increases with the number of sires in the brood primary length) at 12 days of age. A small blood sam- (Whittingham et al. 2006; Dunn et al. 2009) and extra- ple (£50 lL) was collected from all adults and nestlings pair young are more heterozygous than within-pair and stored in lysis buffer at 4 C. All adults were cap- young in comparisons of maternal half-sibs (Stapleton tured in their nest box and identified as the putative et al. 2007). In this study, we found that when experi- parents while feeding chicks. Unhatched eggs and dead enced females were paired with a genetically similar nestlings were collected and tissues were frozen at mate they had more sires in their brood and greater )20 C. We genotyped 94% of all eggs laid (664 ⁄ 706), hatching success. including 12 unhatched eggs.

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extra-pair sire, and thus, determine the total number of Analysis of parentage and genetic similarity sires contributing to each brood. In the remaining In this study, parentage was determined for a total of 138 broods, there were at least two extra-pair young with broods. The number of microsatellite loci used to deter- unknown sires, probably males from outside our study mine parentage varied between years because the nests population. In these cases, we estimated the number of included in this study were control nests from several unknown extra-pair sires by estimating whether the different experiments in previous years. We used eight nestlings in the brood were full- or half-siblings using microsatellite loci in 1999 (total probability of exclusion the likelihood ratio test in the computer program KINSHIP

[Pet] = 0.9996; N = 16 broods; Whittingham et al. 2006), 1.2. We determined the total number of sires in each seven loci in 2000 (Pet = 0.993; N = 58 broods; Dunn et al. brood by combining the number of assigned resident

2009), and four (Pet = 0.996) or eight (Pet = 0.9996) loci in sires and the number of unknown sires. 2001 (N = 30 broods) and 2002 (N = 34 broods; Dunn & Whittingham 2007). For the 2001 and 2002 samples, we Data analysis found it was more efficient to use four loci initially for the paternity exclusion analysis, and then use four more We used ordinal logistic regression to examine whether loci (eight total) to assign extra-pair sires. Details of mi- genetic similarity (estimated by relatedness) of social crosatellite amplification, vizualization, determination of mates influenced the number of sires in a brood within-pair and extra-pair young, and assignment of (mean±SE: 2.38 ± 0.09, N = 138; range 1–6, mode = 2). extra-pair sires are given in Whittingham et al. (2006), In each model, we included year, number of young Dunn & Whittingham (2007), and Dunn et al. (2009). sampled, male and female breeding experience (some ⁄ We compared the genetic similarity of females to their none), and their interactions. In some cases, experienced within-pair and extra-pair mates with estimates of breeders were also sampled as inexperienced breeders, genetic similarity from the computer program KINSHIP 1.2 so in the analyses we included male or female identity (Goodnight & Queller 1999). All comparisons of genetic as variables nested within breeding experience to similarity were based on a total of seven (2000) or eight account for the lack of independence of these observa- (1999, 2001 and 2002) loci. Using the same microsatellite tions. Of 110 different females, 22 were represented in loci to assess parentage and genetic similarity could two broods and three were represented in three broods. result in a false positive relationship between these two Of 106 different males, eight were represented in three variables because the detection of extra-pair young can broods and 16 were represented in two broods. None of increase when the extra-pair sire is more genetically dis- the individuals represented in more than one year were similar to the female than her social mate (Wetzel & socially mated to the same individual in both years. To Westneat 2009). However, these biases are negligible obtain a final model that was simple yet had high pre- when using seven or more loci or mean observed het- dictive power, we sequentially removed variables with erozygosity is >0.60 (Wetzel & Westneat 2009). Our little predictive ability (P > 0.15) using the statistical study met both of these criteria. Furthermore, there was program JMP (SAS Institute 2003). We compared each no indication that the probability of detecting extra-pair model using Akaike’s information criterion corrected young increased when females were more genetically (AICc) for small samples, and the Akaike weight, which dissimilar to their social mate. The number of extra-pair gives the relative likelihood of each model given the young was not related to the genetic similarity of the data (Burnham & Anderson 2002). We considered mod- 2 female and her social mate (v 1 = 0.96, P < 0.33) in an els whose AICc values differed by >4 from the model ordinal logistic regression that also contained the num- with the smallest AICc value (i.e. Di >4) to have consid- ber of young sampled and year. In addition, we tested erably less support (Burnham & Anderson 2002). Means whether any single locus had a disproportionate effect are presented with their SE throughout. on our estimation of genetic similarity by recalculating our estimates and each time leaving out one locus. Results These nine estimates of genetic similarity were highly correlated (mean r = 0.87, all P < 0.0001, range: 0.76– In this study, 82% (113 ⁄ 138) of broods contained extra- 0.97), suggesting that no single locus had a dispropor- pair young, 48% (319 ⁄ 664) of all young were extra-pair, tionate effect on our estimate of genetic similarity. and 56% (180 ⁄ 319) of extra-pair young were assigned to extra-pair sires. Females that produced extra-pair young were genetically more similar (higher related- Number of sires ness, r) to their social partner (mean r: 0.14 ± 0.026) In 42% (47 ⁄ 113) of broods with extra-pair young, we than to their extra-pair mates (0.06 ± 0.020; paired could assign all, or all but one, extra-pair young to an t65 = 2.55, P=0.013; r was averaged for nests with

2010 Blackwell Publishing Ltd BREEDING EXPERIENCE AND POLYANDRY 2331 multiple extra-pair sires). Females that were more simi- lar to their social mate also produced broods sired by a greater number of different males, but this occurred only for experienced females (interaction between female breeding experience and genetic similarity of the 2 social pair, Ordinal logistic regression, v 1 = 5.89, P < 0.01; Table 1, Fig. 1a). In contrast, males with prior breeding experience had fewer sires in their broods (Table 1), but this was primarily driven by one outlier. After deleting this observation, the P value for male breeding experience changed from 0.03 to 0.36, with lit- tle qualitative change to the other variables. Thus, we focused next on female variables, and here the most parsimonious model, based on AICc values, only included genetic similarity, the number of young sam- pled and their interactions with female breeding experi- ence (see reduced model 2, Table 1). The other two models had AICc values >19 higher than reduced model 2 and were >1000 times less likely based on Ak- aike weights. Female age (1 year or older) was not sig- 2 nificant (v 1 = 1.06, P = 0.30) when added to the variables in reduced model 2 (Table 1), and it did not change the other results qualitatively. Although experi- Fig. 1 (a) Genetic similarity of adult pairs in relation to the enced females had more sires, they did not have more number of sires in the brood for experienced (solid line, filled extra-pair young (45 ± 0.05%) than inexperienced circles) and inexperienced (dashed line, open circles) female females (51 ± 0.03%; Wilcoxon Z = 1.1, P = 0.26). tree swallows. (b) Females breeding in 2 years (N = 25) increased the number of sires in a brood when they switched The effect of female breeding experience on the num- to a social partner that was genetically more similar and ber of sires was corroborated in an analysis of the same decreased the number of sires when they switched to a partner female breeding in different years with different social that was genetically less similar. mates. When females had social partners that were genetically more similar, there was an increase in num- ber of sires in her brood (N=25 females; r2 = 0.18,

F1,23 = 5.14, P = 0.03; Fig. 1b). Table 1 Effects of breeding experience (none ⁄ some) and GS of Next, we examined whether the larger number of social pair on the total number of sires per brood sires in broods of experienced females influenced their . Experienced females (N = 53) Reduced Reduced showed a positive relationship between hatching suc- Full model model 1 model 2 cess and the number of sires (0.68 ± 0.37; ordinal logis- 2 Variable v2 P v2 P v2 P tic regression: v 1 = 3.9, P = 0.04), but inexperienced ) 2 females (N = 85) did not ( 0.21 ± 0.24; v 1 = 0.8, N young 7.31 0.12 6.89 0.14 7.07 0.13 P = 0.37; Fig. 2). This difference produced a significant GS of social pair 0.25 0.62 1.41 0.24 0.35 0.55 interaction between female experience and number of Female BE (FBE) 26.35 0.04 26.08 0.05 29.48 0.06 2 sires (ordinal logistic regression: v 1 = 4.1, P = 0.04) in a FBE*GS of social pair 5.89 0.01 5.03 0.03 4.77 0.03 model that also included genetic similarity of the social FBE*No. young 24.79 <0.01 25.70 <0.01 19.6 <0.01 pair ()2.08 ± 1.13; v2 = 3.4, P = 0.06) and the interac- Male BE (MBE) 16.86 0.03 17.23 0.03 —— 1 MBE*GS of social pair 0.24 0.62 — — — — tion between female experience and genetic similarity 2 MBE*No. young 4.29 0.23 — — — — (v 1 = 0.9, P = 0.35). Thus, experienced females had Year 2.95 0.40 — — — — greater hatching success when they had more sires in AICc )264.5 )278.5 )298.0 their brood, and, overall, pairs that were genetically more similar tended to have lower hatching success. GS, genetic similarity; BE, breeding experience. Chi-square and P values are from maximum-likelihood ratio tests using ordinal logistic regression. All analyses included Discussion number of young in the brood and female or male individual identity nested within BE. Significant effects are in bold type. The role of female choice in extra-pair mating and its Sample size was 138 broods for all models. adaptive significance remain controversial (Arnqvist &

2010 Blackwell Publishing Ltd 2332 L. A. WHITTINGHAM and P. O. DUNN

patibility complex-based mate choice in several verte- brate taxa (see Eizaguirre et al. 2009) it remains unknown if it is influenced by female age or breeding experience. It is also possible that older or more experienced females are better able to influence paternity through pre-copulatory mechanisms, particularly how they find and evaluate potential mates. For example, experienced females may travel greater distances during their fertile period and encounter more potential mates, which may also result in finding males that are more genetically Fig. 2 Hatching success increased with the number of sires in dissimilar. In superb fairy-wrens (Malurus cyaneus) the the brood for experienced (solid line, filled circles), but not number of different extra-pair sires in a brood increases inexperienced (dashed line, open circles) female tree swallows. with the distance that females travel away from their own territory (Double & Cockburn 2000). Other studies Kirkpatrick 2007; Griffith 2007; Eliassen & Kokko 2008). have shown that males from more distant locations are However, previous studies have not considered female genetically more dissimilar to females (Reid 2007), and breeding experience or the number of sires in their females produce young with greater heterozygosity analyses. If female breeding experience influences extra- when they mate with distant extra-pair males (Foerster pair mating, then it is not surprising that few studies et al. 2003). Not surprisingly, female tree swallows also have found the predicted benefits of extra-pair mating, travel long distances during their fertile period (Dunn because only a subset of females will realize the benefit. & Whittingham 2005; Stapleton & Robertson 2006) and As predicted, we found that experienced female tree extra-pair mating with distant males results in extra- swallows had more sires in their brood when paired to pair young with greater heterozygosity (Stapleton et al. more genetically similar social mates, and an increase in 2007). Thus, opportunities to mate with extra-pair males polyandry was also associated with greater hatching at greater distances may have an important influence success. Thus, genetic diversification of the brood on the female’s ability to find genetically dissimilar through polyandrous mating appears to positively influ- extra-pair mates and her ability to realize the benefits of ence female fitness, but previous breeding experience extra-pair mating. It is possible that experienced affects the ability of females to realize these benefits. females are more likely to travel greater distances Our results suggest that experienced females are better because they are more familiar with the area or are in able to assess genetic dissimilarity directly or differences better condition (Dunn & Whittingham 2007). in their mating behaviour allow post-copulatory pro- More experienced or older females may also be more cesses of sperm competition to bias fertilization toward likely to have multiply sired broods, because they are more genetically dissimilar (or compatible) males. It is better able to avoid male efforts to guard them or other- possible that this effect was also partly due to age wise constrain extra-pair mating (Brylawski & Whitting- effects, but we found no significant effect of female age ham 2004; Dietrich et al. 2004; Bouwman & Komdeur (SY vs. ASY) in our analyses, and, most of the females in 2005; Johnsen et al. 2008). In tree swallows, males do this study (88%) were at least 2 years old. Indeed, our not guard their mates (Leffelaar & Robertson 1984), but paired analysis of the same female breeding in different the frequency of within-pair copulation is related to years (Fig. 1b) provides strong support for the idea that paternity (Crowe et al. 2009), suggesting that experi- individual females have a change in the number of sires enced females may be better able to manipulate the tim- in response to the genetic similarity of their mate. ing or number of extra-pair copulations so they are If females assess genetic similarity, then the mecha- more likely to result in fertilization. nism is still unclear. A few studies have suggested that Polyandrous mating behaviour has long been associ- females might assess male genetic dissimilarity directly, ated with genetic diversification and the avoidance of perhaps through olfactory cues related to the major his- especially in small, isolated pop- tocompatibility complex (Freeman-Gallant et al. 2003; ulations in which the risk of inbreeding is high (e.g. Richardson et al. 2005, but see Westerdahl 2004). Since Madsen et al. 1992; Reid et al. 2007). However, inbreed- diversity at functional genes such as the major histocom- ing depression has also been documented in outbred patibility complex is likely to have direct effects on populations of birds (Kruuk et al. 2002; Szulkin et al. female fitness, it may be more important in choosing 2007; Townsend et al. 2009). In tree swallows, levels of high quality extra-pair mates, and prior experience of inbreeding appear greater than random, presumably as females may influence this ability. Although there is a a consequence of limited natal dispersal (Shutler et al. growing body of evidence supporting major histocom- 2004) and constrained social mate choice. This may

2010 Blackwell Publishing Ltd BREEDING EXPERIENCE AND POLYANDRY 2333 favour polyandrous mating behaviour which results in thank the Editor and two anonymous reviewers for their com- extra-pair sires that are more genetically dissimilar to ments on the manuscript. This work was approved by the the female than her social mate and greater hatching UWM Animal Care and Use Committee (protocols 98-99#26, 99-00#19, 00-01#10, and 01-02#107). success. By promoting sperm competition, polyandry provides a relatively simple tactic for reducing inbreed- ing depression and increasing offspring genetic compat- References ibility (Zeh & Zeh 1997; Tregenza & Wedell 2000) because it essentially sets up a ‘genetically loaded raffle’ Arnqvist G, Kirkpatrick M (2007) The evolution of infidelity in socially monogamous passerines revisited: a reply to Griffith. whereby sperm competition is biased toward the most American Naturalist, 169, 282–283. genetically compatible male (Griffith & Immler 2009). Bensch S, Hasselquist D, von Schantz T (1994) Genetic There is mounting empirical evidence that under these similarity between parents predicts hatching failure: circumstances the sperm of more dissimilar males is nonincestuous inbreeding in the great reed warbler? more likely to fertilize the female’s eggs in several ani- Evolution, 48, 317–326. mal taxa (Olsson et al. 1996; Zeh & Zeh 1997; Tregenza Bouwman KM, Komdeur J (2005) Old female reed buntings & Wedell 1998, 2002; Stockley 1999; Jehle et al. 2007) (Emberiza schoeniclus) increase extra-pair paternity in their broods when mated to young males. Behaviour, 142, 1449– including birds (Pizzari et al. 2004; Thuman & Griffith 1463. 2005). In tree swallows, fertilization by the sperm of Brylawski AMZ, Whittingham LA (2004) An experimental genetically more dissimilar extra-pair males was associ- study of mate guarding and paternity in house wrens. ated with greater hatching success, which may be the Animal Behaviour, 68, 1417–1424. result of postcopulatory sperm competition. Burnham KP, Anderson DR (2002) Model Selection and Even though a study of tree swallows in Ontario Multimodel Inference: A Practical Information–Theoretic found that extra-pair young were more heterozygous Approach. Springer, New York. Cordero PJ, Aparicio JM, Veiga JP (2004) Parental genetic than within-pair young from the same brood (Stapleton characteristics and hatching success in the spotless starling, et al. 2007), the polyandrous mating behaviour of Sturnus unicolor. Animal Behaviour, 67, 637–642. females in our study suggests that they are attempting Crowe SA, Kleven O, Delmore KE et al. (2009) Paternity to increase the overall genetic diversity of their broods assurance through frequent copulations in a wild passerine (Whittingham et al. 2006). This type of bet-hedging tactic with intense sperm competition. Animal Behaviour, 77, 183–187. would only be successful if additional extra-pair sires Dietrich V, Schmoll T, Winkel W, Epplen JT, Lubjuhn T (2004) led to broods that were more genetically diverse than Pair identity—an important factor concerning variation in extra-pair paternity in the coal tit (Parus ater). Behaviour, 141, average, as it does in tree swallows (Whittingham et al. 817–835. 2006), and if females benefited in terms of greater hatch- Double M, Cockburn A (2000) Pre-dawn infidelity: females ing success (this study; Bensch et al. 1994) or offspring control extra-pair mating in superb fairy-wrens. Proceedings survival (Foerster et al. 2003; Oh & Badyaev 2006). If of the Royal Society B: Biological Sciences, 267, 465–470. females mated with numerous males without any dis- Dunn PO, Whittingham LA (2005) Radio-tracking of female crimination or biases in fertilization (traditional bet- tree swallows prior to egg-laying. Journal of Field Ornithology, hedging), then there would not be any reason to predict 76, 260–264. Dunn PO, Whittingham LA (2007) Search costs influence the that their broods would be any more genetically diverse spatial distribution, but not the level, of extra-pair mating in (e.g. higher heterozygosity) or higher quality (e.g. tree swallows. and Sociobiology, 61, 449–454. greater hatching success) than average (Yasui 1998). In Dunn PO, Lifjeld JT, Whittingham LA (2009) Multiple this case, females would be equally likely to mate with paternity and offspring quality in tree swallows. Behavioral additional males that share the same alleles or have dif- Ecology and Sociobiology, 63, 911–922. ferent ones, resulting in broods with average genetic Dunn PO, Whittingham LA, Lifjeld JT, Robertson RJ, Boag PT diversity. In this study there appeared to be non-ran- (1994) Effects of breeding density, synchrony, and experience on extrapair paternity in tree swallows. Behavioral Ecology, 5, dom choice of mates, as only experienced females had 123–129. more sires in their brood and greater hatching success, Edly-Wright C, Schwagmeyer PL, Parker PG, Mock DW (2007) when they were paired to genetically similar social Genetic similarity of mates, offspring health and extrapair mates. Thus, the benefits to females from multiple mat- fertilization in house sparrows. Animal Behaviour, 73, 367–378. ing may only be revealed when female breeding experi- Eimes JA, Parker PG, Brown JL, Brown ER (2005) Extrapair ence and number of mates are considered. fertilization and genetic similarity of social mates in the Mexican jay. Behavioral Ecology, 16, 456–460. Eizaguirre C, Yeates SE, Lenz TL, Kalbe M, Milinski M (2009) Acknowledgements MHC-based mate choice combines good genes and maintenance of MHC polymorphism. Molecular Ecology, 18, We thank J. Lifjeld and M. Stapleton for their help with field 3316–3329. and lab work as part of other studies of this population. We

2010 Blackwell Publishing Ltd 2334 L. A. WHITTINGHAM and P. O. DUNN

Eliassen S, Kokko H (2008) Current analyses do not resolve Kruuk L, Sheldon BC, Merila J (2002) Severe inbreeding whether extra-pair paternity is male or female driven. depression in collared flycatchers (Ficedula albicollis). Behavioral Ecology and Sociobiology, 62, 1795–1804. Proceedings of the Royal Society B: Biological Sciences, 269, Foerster K, Delhey K, Johnsen A, Lifjeld JT, Kempenaers B 1581–1589. (2003) Females increase offspring heterozygosity and fitness Leffelaar D, Robertson RJ (1984) Do male tree swallows guard through extra-pair matings. Nature, 425, 714–717. their mates? Behavioral Ecology and Sociobiology, 16, 73–79. Freeman-Gallant CR, Meguerdichian M, Wheelwright NT, Leffelaar D, Robertson RJ (1985) Nest usurpation and female Sollecito SV (2003) Social pairing and female mating fidelity competition for breeding opportunities by tree swallows. predicted by restriction fragment length polymorphism Wilson Bulletin, 97, 221–224. similarity at the major histocompatibility complex in a Leffelaar D, Robertson RJ (1986) Equality in feeding roles and songbird. Molecular Ecology, 12, 3077–3083. the maintenance of monogamy in tree swallows. Behavioral Freeman-Gallant CR, Wheelwright NT, Meiklejohn KE, Ecology and Sociobiology, 18, 199–206. Sollecito SV (2006) Genetic similarity, extrapair paternity, Madsen T, Shine R, Loman J, Hakansson T (1992) Why and offspring quality in Savannah sparrows (Passerculus do female adders copulate so frequently? Nature, 355, 440– sandwichensis). Behavioral Ecology, 17, 952–958. 441. Fromhage L, Kokko H, Reid JM (2009) Evolution of mate Mulard H, Danchin E, Talbot SL et al. (2009) Evidence that choice for genome-wide heterozygosity. Evolution, 63, 684– pairing with genetically similar mates is maladaptive in a 694. monogamous bird. BMC Evolutionary Biology, 9, 147. Fossøy F, Johnsen A, Lifjeld JT (2008) Multiple genetic benefits Oh KP, Badyaev A (2006) Adaptive genetic complementarity in of female in a socially monogamous passerine. mate choice coexists with preference for elaborate sexual Evolution, 62, 145–156. traits. Proceedings of the Royal Society B: Biological Sciences, Goodnight KF, Queller DC (1999) Computer software for 273, 1913–1919. performing likelihood tests of pedigree relationship using Olsson M, Shine R, Madsen T (1996) Sperm selection by genetic markers. Molecular Ecology, 8, 1231–1234. females. Nature, 383, 585. Griffith SC (2007) The evolution of infidelity in socially Pedersen MC, Dunn PO, Whittingham LA (2006) monogamous passerines: neglected components of direct Extraterritorial forays are related to a male ornamental trait and indirect selection. American Naturalist, 169, 274–281. in the common yellowthroat. Animal Behaviour, 72, 479–486. Griffith SC, Immler S (2009) Female infidelity and genetic Pizzari T, Løvlie H, Cornwallis C (2004) Sex-specific, compatibility in birds: the role of the genetically loaded counteracting responses to inbreeding in a bird. Proceedings raffle in understanding the function of extrapair paternity. of the Royal Society B: Biological Sciences, 271, 2115–2121. Journal of Avian Biology, 40, 97–101. Puurtinen M, Ketola T, Kotiaho JS (2009) The good-genes and Griffith SC, Owens IPF, Thuman KA (2002) Extra pair compatible-genes benefits of mate choice. American paternity in birds: a review of interspecific variation and Naturalist, 174, 741–752. adaptive function. Molecular Ecology, 11, 2195–2212. Reid J, Arcese P, Keller L et al. (2007) Inbreeding effects on Hansson B, Hasselquist D, Bensch S (2004) Do female great immune response in free-living song sparrows (Melospiza reed warblers seek extra-pair fertilizations to avoid melodia). Proceedings of the Royal Society B: Biological Sciences, inbreeding? Biology Letters, 271, S290–S292. 274, 697–706. Hussell D (1983) Age and plumage color in female tree Reid JM (2007) Secondary sexual ornamentation and non- swallows. Journal of Field Ornithology, 54, 312–318. additive genetic benefits of female mate choice. Proceedings of Jehle R, Sztatecsny M, Wolf JBW et al. (2007) Genetic the Royal Society B: Biological Sciences, 274, 1395–1402. dissimilarity predicts paternity in the smooth newt Robertson RJ, Rendell WB (1990) A comparison of the breeding (Lissotriton vulgaris). Biology Letters, 3, 526–528. ecology of a secondary cavity nesting bird, the Tree Swallow Jennions M, Petrie M (2000) Why do females mate multiply? A (Tachycineta bicolor), in nest boxes and natural cavities. review of the genetic benefits. Biological Reviews, 75, 21–64. Canadian Journal of Zoology, 68, 1046–1052. Johnsen A, Pa¨rn H, Fossøy F et al. (2008) Is Robertson RJ, Rendell WB (2001) A long-term study of constrained by the presence of her social mate? An reproductive performance in tree swallows: the influence of experiment with bluethroats Luscinia svecica. Behavioral Ecology age and senescence on output. Journal of Animal Ecology, 70, and Sociobiology, 62, 1761–1767. 1014–1031. Keller LF, Grant PR, Grant BR, Petren K (2002) Environmental Robertson RJ, Stutchbury BJ, Cohen RR (1992) Tree swallow. conditions affect the magnitude of inbreeding depression in In: The Birds of North America, no. 11 (eds Poole A, survival of Darwin’s finches. Evolution, 56, 1229–1239. Stettenheim P, Gill F), pp. 1–28. Academy of Natural Kempenaers B (2007) Mate choice and genetic quality: a review Sciences, Philadelphia, Pennsylvania. of the heterozygosity theory. Advances in the Study of SAS Institute (2003) jmp 5.0.1 User’s Guide. SAS Institute, Cary, Behavior, 37, 189–278. North Carolina. Kempenaers B, Adriaensen F, van Noordwijk AJ, Dhondt AA Schmoll T, Quellmalz A, Deitrich V et al. (2005) Genetic (1996) Genetic similarity, inbreeding and hatching failure in similarity between pair mates is not related to extrapair blue tits: are unhatched eggs infertile? Proceedings of the Royal paternity in the socially monogamous coal tit. Animal Society B: Biological Sciences, 263, 179–185. Behaviour, 69, 1013–1022. Krokene C, Lifjeld JT (2000) Variation in the frequency of Shutler D, Hussell DJT, Horn AG et al. (2004) Breeding extra-pair paternity in birds: a comparison of an island and between tree swallows from the same brood. Journal of Field a mainland population of blue tits. Behaviour, 137, 1317–1330. Ornithology, 75, 353–358.

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Simmons LW (2005) The evolution of polyandry: sperm Tregenza T, Wedell N (1998) Benefits of multiple mates in the competition, sperm selection and offspring viability. Annual cricket . Evolution, 52, 1726–1730. Review of Ecology Evolution and Systematics, 36, 125–136. Tregenza T, Wedell N (2000) Genetic compatibility, mate Stapleton M, Robertson RJ (2006) Female tree swallow home- choice and patterns of parentage: Invited Review. Molecular range movements during their fertile period as revealed by Ecology, 9, 1013–1027. radio-tracking. Wilson Journal of Ornithology, 118, 502–507. Tregenza T, Wedell N (2002) Polyandrous females avoid costs Stapleton M, Kleven O, Lifjeld J, Robertson R (2007) Female of inbreeding. Nature, 415, 71–73. tree swallows (Tachycineta bicolor) increase offspring Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: heterozygosity through extrapair mating. Behavioral Ecology causes, correlates, and conflict. Annual Review of Ecology and and Sociobiology, 61, 1725–1733. Systematics, 34, 365–396. Stockley P (1999) Sperm selection and genetic incompatibility: Wetzel DP, Westneat DF (2009) Heterozygosity and extra-pair does relatedness of mates affect male success in sperm paternity: biased tests result from the use of shared markers. competition? Proceedings of the Royal Society B: Biological Molecular Ecology, 18, 2010–2021. Sciences, 266, 1663–1670. Whittingham LA, Dunn PO, Stapleton MK (2006) Repeatability Suter SM, Keiser M, Feignoux R, Meyer DR (2007) Reed of extra-pair mating in tree swallows. Molecular Ecology, 15, bunting females increase fitness through extra-pair mating 841–849. with genetically dissimilar males. Proceedings of the Royal Yasui Y (1998) The ‘genetic benefits’ of female multiple mating Society B: Biological Sciences, 274, 2865–2871. reconsidered. Trends in Ecology and Evolution, 13, 246. Szulkin M, Garant D, McCleery RH, Sheldon BC (2007) Zeh JA, Zeh DW (1997) The evolution of polyandry II: post- Inbreeding depression along a life-history continuum in the copulatory defences against genetic incompatibility. great tit. Journal of Evolutionary Biology, 20, 1531–1543. Proceedings of the Royal Society B: Biological Sciences, 264, 69–75. Tarvin KA, Webster MS, Tuttle EM, Pruett-Jones S (2005) Genetic similarity of social mates predicts the level of extrapair paternity in splendid fairy-wrens. Animal Behaviour, The authors are interested in avian ecology and evolution, par- 70, 945–955. ticularly extra-pair mating and its effect on . Thuman KA, Griffith SC (2005) Genetic similarity and the Current studies focus on swallows, warblers, and grouse, and nonrandom distribution of paternity in a genetically highly use a variety of molecular genetic techniques. This work is part polyandrous shorebird. Animal Behaviour, 69, 765–770. of a long-term study of the adaptive significance of multiple Townsend AK, Clark AB, McGowan KJ et al. (2009) Disease- mating in tree swallows by professors Linda Whittingham and mediated inbreeding depression in a large, open population Peter Dunn. of cooperative crows. Proceedings of the Royal Society B: Biological Sciences, 276, 2057–2064.

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