Partner switching can favour cooperation in a biological market.

doi: 10.1111/jeb.12455

Partner switching can favour cooperation in a biological market P. L. SCHWAGMEYER Department of Biology, University of Oklahoma, Norman, OK, USA

Keywords:

Abstract

biological market; by-product benefits; cooperation; house sparrows; mutualism; partner dismissal; partner fidelity feedback; partner switching; Passer domesticus.

Intraspecific cooperation and interspecific mutualisms can be promoted by mechanisms that reduce the frequency with which cooperative organisms are exploited by unhelpful partners. One such mechanism consists of changing partners after interacting with an uncooperative individual. I used McNamara et al.’s (Nature, 451, 2008, 189) partner switching model as a framework to examine whether this mechanism can select for increased cooperative investment by house sparrows (Passer domesticus) collaborating to rear offspring; previous research on this species has shown that substantial cooperative investments by both pair members are required to achieve high pay-offs from collaborating. I found that the poorer the outcome of a breeding attempt relative to the number of eggs the female invested, the greater the likelihood of partner switching. The incidence of partner switching changed seasonally, with peak switching coinciding with an increase in the number of alternative partners available to females. After females switched partners, their breeding outcomes rose to match those of females that remained with the same partner; this was not the case for males that switched partners. Consistent with the model’s prediction, males in stable partnerships achieved over 25% higher than average reproductive success, which was attributable to both persistently good breeding outcomes and their older partners’ high fecundity. These results provide empirical support for the hypothesis that partner switching favours increased cooperative investment levels, and they demonstrate that variation in the relative value of by-product benefits can enhance that process.

Introduction When unrelated individuals collaborate on tasks, there commonly exist short-term gains to individuals that exploit their partners. Cooperation can still be advantageous in such contexts, however, if individuals that fail to contribute to the common good can be induced to become more cooperative (e.g. by punishment: Clutton-Brock & Parker, 1995; rewards: Axelrod & Hamilton, 1981; threats: Cant, 2011) or if other mechanisms exist that preserve or encourage alliances among individuals that are most likely to cooperate (Queller, 1985, 2011; Lehmann & Keller, 2006; Fletcher & Doebeli, 2009; Leimar & Hammerstein, 2010). For example, if an individual’s level of cooperative investment is Correspondence: P. L. Schwagmeyer, Department of Biology, University of Oklahoma, Norman, OK 73019, USA. Tel.: 804 708 0874; e-mail: [email protected]

reliably associated with some cue, then choice of partners prior to collaboration can provide a selective advantage to cooperation (Parker, 1983; No€ e, 1990; Bull & Rice, 1991). Alternatively, when individuals have the opportunity to interact repeatedly, then even if individuals initially choose their associates randomly, refusing further collaboration with those that contribute very little can enhance the evolutionary stability of cooperation (Batali & Kitcher, 1995; McNamara et al., 2008; Izquierdo et al., 2010). Several of the mechanisms that have been identified as potentially important for facilitating cooperation may apply when two mating partners collaborate to rear offspring. Biparental investment is particularly well suited for testing hypotheses regarding cooperation between unrelated individuals because the goods and services each partner contributes are channelled directly into reproduction. As a result, the fitness consequences of variable levels of investment can be estimated, and

ª 2014 THE AUTHOR. J. EVOL. BIOL. 27 (2014) 1765–1774 JOURNAL OF EVOLUTIONARY BIOLOGY ª 2014 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY

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possible mechanisms for maintaining cooperation can be evaluated in terms of their impact on the reproductive fates of the relevant parties. In this investigation, I applied the model of McNamara et al. (2008) to test whether partner switching is able to produce a selective advantage for increased cooperative investment. I used data from a 7-year study of house sparrows (Passer domesticus), and I focused largely on the potential fitness consequences of partner switching, rather than the causes. McNamara et al.’s (2008) model is structured such that individuals collaborate with a partner on a shared task and then reproduce in proportion to their combined contributions. After reproducing, each party chooses whether to continue the partnership. The model features coevolution of the threshold for partner switching and the mean cooperative effort in the population: as the average level of cooperation increases, individuals must expend greater effort to avoid being dismissed. McNamara et al. (2008) found that, even if individuals initially choose partners randomly, partner dismissal can increase the equilibrium level of cooperative behaviour. Three characteristics of the sparrows conform closely to the assumptions and structure of the model. First, a pair can produce up to four broods per season (Schwagmeyer & Mock, 2003); thus, there exist opportunities for repeated interactions within a breeding season as well as from 1 year to the next. Second, McNamara et al. (2008) used both the standard Prisoner’s Dilemma and the Snowdrift game pay-offs in their analyses. As they point out, the pay-off function for the Snowdrift game played in continuous form is appropriate for biparental care, where the net gain an individual receives from collaboration hinges on the summed contributions of the two parents minus the costs to the individual. Several aspects of house sparrow breeding success – including the number of nestlings that survive to fledge, offspring mass at fledging and the number of offspring per brood that survive to breeding age – are known to be positive functions of parental provisioning behaviour (Schwagmeyer & Mock, 2008; Mock et al., 2009; Schroeder et al., 2013). Third, the model assumes that an individual’s level of cooperative investment persists across its lifetime; thus, in this model, partner switching does not transform previously exploitative individuals into cooperators, as it does in some situations (e.g. Bshary & Grutter, 2005), nor is cooperation a conditional strategy, as it is in some partner switching models (e.g. Izquierdo et al., 2010). Further, McNamara et al. (2008) showed that the ability of partner switching to select for increased cooperation is contingent on the degree to which individuals differ in their levels of cooperative effort. Thus, both variation among individuals in the quality or quantity of contributions they offer and consistency across time in the contribution levels of individuals are required (McNamara et al., 2008): individuals would have little to gain from rejecting a partner if the partner’s past contributions

are independent of its future contributions or if there are no alternative partners offering higher investment levels. House sparrows meet these requirements in that the provisioning behaviour of male sparrows is repeatable across breeding episodes (Schwagmeyer & Mock, 2003; Nakagawa et al., 2007a). Although the repeatability of female provisioning is relatively low (Schwagmeyer & Mock, 2003; Nakagawa et al., 2007a), and variation among females in mean provisioning level is substantially less than variation among males (Schwagmeyer & Mock, 2003), there exist both individual and age-related variation in aspects of female fecundity (Hatch & Westneat, 2007; Nakagawa et al., 2007b; Westneat et al., 2009). The sparrows do not conform to all properties of McNamara et al.’s (2008) model, however. One obvious difference is that the types of investments provided by each member of a pair are not identical: females contribute clutches as well as parental care. In addition, females have more alternative partners available than do males (see below), so it is consequently unlikely that the sexes pay equal costs of searching for a new partner. Such asymmetries are common features of what have been termed ‘biological markets’ (No€ e et al., 1991; No€ e & Hammerstein, 1994, 1995). Biological market theory draws on models and principles developed by economists, and it is useful in predicting how the nature of interactions between individuals belonging to two discrete classes is modified by changes in the relative value of the resources and services they exchange (No€ e & Hammerstein, 1994, 1995; No€ e, 2001). It has been applied to analyses of intraspecific cooperation [e.g. modifications of the reciprocity of allogrooming exchanges in relation to a partner’s ability to offer social tolerance (Port et al., 2009) or food (Fruteau et al., 2009)], as well as mutualisms (e.g. preferential treatment by cleaner fish of particular types of clients: Bshary & Grutter, 2002; control of uncooperative rhizomes in rhizobial-legume mutualisms: Simms et al., 2006). I relied on a biological market perspective in two respects. First, market effects created by the sparrows’ sex differences in the availability of alternative partners are predicted to place females in the class of ‘choosers’ or ‘rejectors’, even if every female offers identical contributions to partnerships (No€ e & Hammerstein, 1994). Although both sexes initiate partner switching in some avian species (e.g. Heg et al., 2003; Moody et al., 2005), I sidestepped the problem of attempting to infer which individual terminated a partnership (see C ezilly et al., 2000) and simplified the analyses by initially assigning that control to females. (I also address the possibility that partner dismissal is practiced by males, however). Second, a biological market approach has often been used to predict facultative responses of individuals to variation in the market value of resources that partners offer, but to capture the coevolution of partner dismissal thresholds and


Partner switching can favour cooperation

cooperative investment, McNamara et al. (2008) assumed that dismissal thresholds as well as investment levels remain stable over individual lifetimes. By contrast, I found that the probability that sparrow pairs switch partners varies seasonally, and I consider market fluctuations as a potential source of the observed change in the partner dismissal threshold. I examined three aspects of house sparrow partner switching in the context of McNamara et al. (2008). First, their model is based on the premise that dissolution of partnerships is contingent on evidence of unsatisfactory partner contributions as revealed by the payoff achieved from collaboration, and I quantified the incidence of partner switching as a function of the success of the pair’s previous reproductive attempt. Second, because partner switching must be advantageous to at least one pair member if it is to result in selection for higher levels of cooperative investment, I tested the prediction that females experience a more favourable outcome once they change partners. Third, I used estimates of the number and quality of offspring produced annually by males to test the key prediction of the model: if partner switching can increase the mean level of cooperative investment in the population across time, then nondismissed individuals should eventually outreproduce rejected individuals, even if nondismissed individuals pay higher costs by contributing more towards each collaboration.

Materials and Methods

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Although the adult sex ratio during the study was roughly 1:1, the operational sex ratio was male-biased. This was partly due to sex differences in mortality rate (e.g. after their first breeding attempt of the season, an average of 35.6 0.10% SD of females died or disappeared each year vs. 20.1 0.07% SD of males), and partly due to variation among surviving females in the number of times they attempted to breed each year (range = 1–4). As a consequence of these two factors, once a female completed at least one breeding cycle during the year, she had an average of 2.8 1.78 SD (N = 244 cases) unpaired males available in her neighbourhood if she were to seek an alternative partner for her next attempt of that season (Appendix SI, A). The pool of available partners expanded for such females each spring (x = 7.6 2.90 SD males per neighbourhood, N = 66 cases) as new males established residency at the site. Although these older females were outnumbered by females breeding on the site for the first time (x% older females = 29.4 4.76 SD), older females initiated reproduction at a time when many males remained unpaired (x = 25 8.2 SD days earlier than first-year females, N = 6 years). The earlier breeding dates of older females were accompanied by an increased number of breeding attempts per year relative to first-year females (x = 2.5 0.92 SD, N = 69 female years for older females vs. x = 1.7 0.84 SD, N = 166 first-year females), and older females also had larger clutch sizes, as in other populations of this species (Nakagawa et al., 2007b; Westneat et al., 2009).

Study species House sparrows are nonmigratory and multibrooded. Although pairs defend the immediate vicinity of their nest from conspecifics, they do not defend feeding territories. For this study, I used data collected during 2000–2006 on adults residing in a nestbox population located in Norman, OK, USA. Nestboxes were censused twice weekly to determine clutch initiation dates, clutch size, hatching success and nestling survival. Chicks were banded and weighed to the nearest 0.1 g eleven days after hatching. Nearly all nestbox residents were individually identifiable by colour bands on their legs. Although we captured individuals to band them and take a small blood sample, the birds at this site were largely unmanipulated during these particular years. I excluded data from one pair that deserted their nest and switched partners after both pair members were inadvertently captured (for banding) nearly simultaneously on the same afternoon. I also excluded from analyses data from the 12.5% (37/297) of pairs which included a polygynous male. Veiga (1990) has shown that the breeding success of such pairs is jeopardized by interference from the male’s other mate; furthermore, the repeatability of polygynous male parental care has not been evaluated.

Definitions I reserved the term ‘partner switching’ for cases where both members of a pair survived sufficiently long to initiate another breeding attempt, but at least one individual paired with a different partner; 35 socially monogamous pairs met this criterion over the 7 years. Partner switches and cases of mate retention were further classified as having occurred ‘overwinter’ (the female did not breed again until the next year) vs. ‘within-season’ (the female had at least one more breeding attempt in the current year). Some individuals also formed a new partnership after a previous mate had died or disappeared. I had no way of knowing whether these individuals would have switched partners if their previous mate had survived, and for most comparisons, I included data from them in a separate group. In these cases, data on surviving pair members were classified as ‘within-season’ if they bred again in the same year after the death or disappearance of a mate, or ‘overwinter’ if their next breeding attempt did not occur until the following spring. Individuals in the overwinter group thus were at least 2 years old, whereas within-season individuals represented a mixture of first-year residents and older birds.


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In McNamara et al. (2008), an individual that invests effort level x requires a minimum fitness pay-off per round of interaction to retain its current partner, and for the Snowdrift game, these fitness pay-offs are a positive function of the summed efforts of the two partners. To estimate the reproductive pay-off from each breeding attempt, I relied on previous results from our local population that showed that the number of chicks in a brood that survive to breeding age is a positive function of both their mean mass on day 11 post-hatch and the number alive on that day (Schwagmeyer & Mock, 2008); I consequently calculated the outcome of a breeding attempt as the product of the two variables. Both mean mass and the proportion of offspring surviving to day 11 are positively related to parental provisioning (Schwagmeyer & Mock, 2008; Mock et al., 2009), and I verified that breeding outcomes are a positive function of each sex of parent’s provisioning behaviour (Appendix S1, B) by applying regression analyses to data from Schwagmeyer & Mock (2008). Breeding outcome values in the current study ranged from 0 (complete breeding failure on the attempt) to ~ 136 (e.g. five chicks weighing an average of 27.2 g each). [It is also possible to estimate the fitness pay-off (number of offspring surviving to breeding age) from a breeding attempt based on parental provisioning data (Schwagmeyer & Mock, 2008), but we had collected parental care data during only a small fraction of the > 250 breeding attempts included in these analyses]. I estimated the annual reproductive success of males as the sum of the outcomes of each breeding attempt of a male in a year; males that nested in an inaccessible site (such that the mass and number of surviving chicks were unknown) during one or more breeding attempts in a season were deleted from the analyses. This measure of annual reproductive success does not include either paternity gains or losses due to extrapair fertilization: the main opportunity cost of male parental care in our local population appears to be a reduction in the incidence of polygyny, rather than a lower likelihood of obtaining extrapair fertilizations (Schwagmeyer et al., 2012). Further, paternity losses are skewed towards polygynous males (Schwagmeyer et al., 2012), which were excluded from these analyses. However, because extrapair fertilization success is strongly biased towards older males (Wetton et al., 1995; Schwagmeyer et al., 2012), overwintering males collectively are likely to have had higher reproductive success than is represented here. Average male reproductive success was set to one for each year of the study based on records from 21 to 30 males per year and a total of 112 different males (see Appendix S1, C); males that bred a single time on the site and then died or disappeared (such that they had no opportunity to be retained as a mate, to switch partners or to pair again after partner death) were eliminated in calculating these annual averages. The standard against which males are evaluated thus is

biased towards individuals that were disproportionately likely to have contributed to the next year’s pool of recruits. Mean clutch size, mean number of offspring surviving to day 11 post-hatch and number of breeding attempts during the season were mean-centred for each year (Appendix S1, C). To evaluate the effects of partnership changes occurring at different times of year, I used measures of the males’ relative success during the following year if partner switching, death of the female or mate retention occurred overwinter, and data from the same year for males that retained the same mate throughout a breeding season or switched partners or whose partner died during the season. Prior to analyses, I eliminated duplicate data from the same individual in the same year (e.g. if a male switched partners overwinter, but retained the same mate throughout the next season; if a male had one mate die but also switched partners within a season), with priority given to retaining categories with the smallest sample sizes (overwintering males and males that switched partners). Statistical analyses SAS version 9.2 was used for data analyses. Generalized linear mixed models (GLMM) with binomial error structures were used for analyses involving binary and proportional response variables, and linear mixed models (LMM) were used when response variables were continuously distributed. LMMs were fit via restricted maximum likelihood, and GLMMs were based on residual pseudo-likelihood estimation. Random effects for each model and their covariance structures are listed in the supplementary information (Appendix S1, C). Initial models included season (overwinter vs. within-season) and the interaction between season and pairing status (retained same mate, experienced partner death, switched partners). Analyses of mean breeding outcomes additionally included mean-centred clutch size and its quadratic term as a covariate, along with interactions among clutch size, pairing status and season. Nonsignificant interaction terms and nonsignificant effects of season or clutch size were removed from final models. Denominator degrees of freedom for mixed models were calculated using the Kenward–Roger method. Denominator degrees of freedom used in pairwise comparisons were adjusted to accommodate variation in the denominator degrees of freedom across least square mean differences, and Dunnett’s T3 tests were used for assessing their significance.

Results Predictors of partnership dissolution Prior to switching partners, females had experienced significantly poorer breeding outcomes, relative to the



size of the clutch they had laid, than females that retained their mate; the mean breeding outcome of females whose mate subsequently died was intermediate (Fig. 1a; LMM main effect of female status: F2,267 = 4.86, P = 0.0085; covariates of mean-centred clutch size and its quadratic term: F1,268 = 26.91, P < 0.0001; F1,267 = 7.32, P = 0.0073). Logistic regression showed that the probability of partner switching increased with declines in breeding attempt outcomes (F1,222 = 10.44, P = 0.0014, N = 95 females, 225

Breeding attempt outcome

(a) 100

a a,b

80

b

60

40

Next breeding attempt outcome

breeding attempts). In addition, time in season had a pronounced effect on the incidence of partner switching (GLMM: F1,64.84 = 10.17, P < 0.0001), such that the least square mean proportion of pairs switching partners increased from 0.077 0.028 SE within a season to 0.405 0.110 SE overwinter. There was no indication that the slope of the relationship between breeding outcome and probability of partner switching differed with time in season (F1,167.5 = 1.19, P = 0.277); rather, the threshold for partner switching changed seasonally (Appendix S1, D1). Because some pairs (including 43% of those that switched partners) had had multiple breeding attempts together, I also examined each pair’s running average outcome for the year as a predictor of partner switching. The results were very similar to those based on the most recent breeding attempt (main effect of average breeding outcome: F1,184.8 = 10.03, P = 0.0018, N = 95 females; main effect of time in season: F2,74.35 = 10.88, P < 0.0001; interaction: F1,221 = 0.01, P = 0.94; Appendix S1, D2). Effects of partner switching on females

Same

Partner died

Switched

(b) 100 a

80

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a

a

In contrast to the outcome of their previous breeding attempt, the average pay-off from the next breeding attempt of females that switched partners did not differ significantly from the mean outcomes achieved by females that retained the same partner and by females that paired with a new mate after death of a partner (Fig. 1b; LMM main effect of female status: F2,238 = 0.42, P = 0.656; covariates of mean-centred clutch size and its quadratic term: F1,237 = 38.29, P < 0.0001; F1,236 = 13.25, P = 0.0003). Consequences of partner switching for males

60

40

Same

Partner died

Switched

Fig. 1 (a) Least square mean breeding attempt outcome (+ 95% CI), adjusted for female clutch size, for females that subsequently retained the same partner for their next breeding attempt (same), switched partners (switched), or had their partner die/disappear (partner died). Means with different letters differ significantly. N = 103 females, 276 breeding attempts (35 partner switches, 50 cases in which a female’s mate died/disappeared, 191 partner retentions). (b) Least square mean outcome (+ 95% CI), adjusted for female clutch size, of the breeding attempt after females retained their partner, paired with a new male following the death of their mate or switched partners. N = 97 females, 245 breeding attempts. Least square mean differences plus 95% adjusted CIs: switched vs. same = 0.4 ( 14.5, 13.8); switched vs. partner died = 5.1 ( 22.37, 12.25); same vs. partner died = 4.7 ( 17.39, 7.97).

The relative annual reproductive success of males varied with their pairing status (Fig. 2; LMM main effect of male status: F2,162 = 9.39, P = 0.0001). Males that retained the same mate throughout a breeding season or retained the same mate from 1 year to the next had significantly higher relative success than either males that switched partners (P = 0.0007) or males experiencing partner death (P = 0.0025); the success achieved by males that lost a partner through death vs. partner switching did not differ significantly (P = 0.6804). Independently of pairing status, the time of year when partnerships were subject to termination also affected male success, with overwintering males attaining approximately 20% higher relative success than within-season males (LMM main effect of season: F1,157 = 5.71, P = 0.0181). These differences in male success derived from variation in multiple components of breeding performance. First, the mean mass of 11-day-old nestlings differed significantly among males of different pairing status (Fig. 3; LMM: F2,109 = 3.66, P = 0.0289), with males in


P. L. SCHWAGMEYER

Annual reproductive success

1.4

a

11

1.2 b

b

1

0.8

0.6

Same

Partner died

Switched

Fig. 2 Least square mean (+ 95% CI) estimated relative annual reproductive success of males that switched partners, had their partner die/disappear or retained the same mate. Male success was defined as the product of the total # fledged young produced annually and their mean mass, with the average for each year of the study set to 1.0. When males retained the same mate, switched partners or had a partner die/disappear while breeding was ongoing, data are based on each male’s mean relative success for that season; when partner switches, death of the female, or mate retention occurred overwinter, data were from each male’s relative success during the following year. Columns labelled with different letters differed significantly. Results are based on 104 males, 161 male years, with 28 partner switches, 59 cases in which a male’s mate died/disappeared and 74 cases of mate retention.

stable partnerships tending to produce broods of heavier chicks than average. The increased mass of their nestlings helped elevate the mean clutch-size-adjusted outcome of these males’ breeding attempts to an aboveaverage level (Fig. 3; LMM main effect of pairing status: F2,156 = 3.59, P = 0.0298; covariates of mean-centred clutch size and its quadratic term, F1,156 = 19.57, P < 0.0001; F1,156 = 8.50, P = 0.0041). Thus, the disparities in clutch-size-adjusted outcomes shown in Fig. 1a (switched partners vs. same) persisted through the breeding season for within-season males and carried over to the next season for overwintering males. Beyond these effects, there were significant differences among the three groups of males in their partners’ ages (Appendix S1, E) and corresponding disparities in partner fecundity. Largely due to overwintering individuals, males that remained paired to the same female had older females as partners on about half of their breeding attempts (least square mean proportion = 0.55 0.086 SE). In turn, the clutches that males in stable partnerships tended were significantly larger than average (Fig. 4), and their mates began laying 6.3 2.15 SE days earlier in the spring than the yearly average (t158 = 2.93, P = 0.0039). By contrast, neither males whose partner died nor males that switched partners had older female partners very often (least square mean proportion, partner died = 0.24 0.057 SE; switched partners: 0.19 0.067 SE), and the timing of the first breeding attempts of males that switched partners and

Relative mean mass, outcome

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P = .013

6 1

P = .821 P = .063

P = .117

P = .157 P = .467

–4 –9 –14

Same

Partner died

Switched

Fig. 3 Light bars: least square mean (+ 95% CI) nestling mass per brood (at day 11 post-hatch) of males that switched partners, experienced partner death/disappearance or retained the same mate. Results are based on 104 males, 155 male years, with 25 partner switches, 57 cases of partner death/disappearance and 73 cases of mate retention. Dark bars: least square mean breeding outcome for the season (+ 95% CI) adjusted for mean clutch size. Results are based on 104 males, 161 male years, with 28 partner switches, 59 cases in which a male’s mate died/disappeared and 74 cases of mate retention; P values indicate whether column means differed significantly from overall mean-centred average for that year (dotted line).

those whose previous partner had died did not differ from the average (first-egg dates, partner switched: x = 1.7 3.50 SE days later than average, t158 = 0.49, P = 0.625); partner died: x = 1.5 2.41 SE days earlier than average, t158 = 0.61, P = 0.543). Partner switching overwinter effectively delayed the onset of breeding relative to what it would have been if males had not switched partners: the new mates of these males began laying their first clutch a mean of 18.4 23.48 SD days later than the males’ former partners (paired t15 = 3.14, P = 0.0067), and overall, the clutches of males that switched partners were smaller than average (Fig. 4). Finally, the number of breeding attempts per year varied with male pairing status (LMM main effect of status: F2,157 = 3.95, P = 0.0212), in addition to being independently associated with an advantage for overwintering males (LMM main effect of season: F1,157 = 5.06, P = 0.0259). Males that retained the same partner were once again favoured and bred more frequently than average (Fig. 4). Males could potentially offset deficiencies in the number and/or quality of offspring they produce per breeding attempt by acquiring multiple mates. However, the frequency with which males that were socially monogamous during one breeding attempt became polygynous on the next was extremely low (6/219 breeding attempts) and unrelated to whether the attempt culminated in mate retention or partner switching (GLMM: F1,217 = 0.01, P = 0.9115).


Relative clutch size, # Breeding attempts


0.5 0.4 0.3

P = .0003 P = .030 P = .756

P = .636

0.2

P = .642

0.1

P = .041

0 –0.1 –0.2 –0.3 –0.4 –0.5

Same

Partner died

Switched

Fig. 4 Light bars: least square mean (+ 95% CI) relative clutch size of males that had a partner die/disappear, males that switched partners and mate-retained males. Dark bars: least square mean (+ 95% CI) number of breeding attempts per season for males that switched partners, had a partner die/disappear and retained the same mate. P values indicate whether column means differed significantly from overall mean-centred average for that year (dotted line). Results are based on 104 males, 161 male years, with 28 partner switches, 59 cases in which a male’s mate died/ disappeared and 74 cases of mate retention.

Discussion These results show that partner switches were preceded by breeding attempts that yielded inferior outcomes relative to the size of the clutch females had contributed. Such deficiencies in the final product of a collaboration could conceivably provide an incentive for either or both individuals to switch partners. However, the results revealed that only females – the class of individuals that had the larger supply of alternative partners – derived an advantage from switching. In particular, after switching partners, females were able to obtain returns on their investments that matched those of comparably experienced females. By contrast, males that switched partners fared poorly, and it is difficult to see how selection would favour male-initiated partner switching. If partner switching is to select for increased cooperative investment, there also must exist fitness advantages for individuals that avoid being dismissed (McNamara et al., 2008). Such benefits are clearly present for male house sparrows: males in stable partnerships achieved over 25% higher estimated reproductive success than their peers, and this advantage was not associated with a reduced likelihood of becoming polygynous. As expected given their previous breeding outcomes and the repeatability of male provisioning behaviour, their mean breeding outcome for the season relative to the average clutch size of their mates was better than average, partially due to the production of offspring that were of marginally higher mass. Moreover, males in

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stable partnerships were paired to females that began breeding relatively early, furnished larger than average clutches and produced more clutches per season. By contrast, males that switched partners as well as those whose previous partner had died were left with replacement mates that laid clutches of either belowaverage or average size. The difference in reproductive success of males that remained with the same mate and those that switched partners therefore combines two effects: the impact of persistently higher breeding outcomes and the contribution to male fitness of increased partner fecundity. The origins of the fitness benefits males obtain from partner retention were most clearly evident among overwintering pairs, whose previous (within-season) breeding outcomes had been sufficiently high to avoid partner switching (Fig. 1a). This previous success then carried over to the following year. A portion of that next year’s reproductive success consequently represents partner fidelity feedback, wherein cooperation during one round of interactions with a partner creates future cooperative benefits from the partnership (sensu Bull & Rice, 1991; Sachs et al., 2004). In particular, the partners of these males were now older, such that they bred often and laid large clutches. These age-related increases in female fecundity are likely to have evolved largely because they serve the interests of females (being extremely common in female vertebrates and occurring even in species in which males provide no post-insemination parental investment); thus, the multiplicative impact they had on the males’ high clutchsized-adjusted breeding outcomes for the year can be considered a one-way by-product benefit (Sachs et al., 2004). Finally, relative to within-season males, overwintering males collectively had higher annual reproductive success, perhaps simply because they participated in more breeding attempts than within-season males. The source of this advantage merits further attention. McNamara et al. model (2008) assumes that an individual’s dismissal threshold remains fixed over its lifetime, such that if partners collaborate once and find each other acceptable, they remain together until one dies. By contrast, around 40% of all partner switches occurred after a pair had had two or more breeding attempts together, and the threshold for sparrow partner switching changed seasonally. This seasonal shift, and the associated five-fold increase in the incidence of partner switching, may occur for several reasons. For example, there are multiple nonadaptive hypotheses for why avian partner switching might be especially common among overwintering birds (Dhondt & Adriaensen, 1994; Choudhury, 1995). Alternatively, there may be selective mortality of within-season birds that have low propensities for switching, such that the overwinter sample is biased towards individuals that switch unless breeding outcomes are high. Yet, a third possibility is


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that market effects may account for the increased breeding outcomes required for overwintering pairs to avoid partner switches. Notable changes occur in the population at this time. For one thing, the supply of unpaired birds of each sex expands in the spring with the influx of first-year individuals, and this should generally reduce any costs to overwintering birds of searching for alternative partners (McNamara et al., 2008). But simultaneously, the composition of the pool of prospective partners is modified. The relative increase in the proportion of first-year females in the pool of unpaired individuals seems unlikely to be of value to overwintering males; however, a male that dismisses his current mate over the winter and searches randomly for another could easily end up exchanging his older partner for a younger one, and she is unlikely to be ready to breed as early in the season or to lay relatively large clutches. On the other hand, the composition of the pool may shift in more desirable ways for overwintering females. First-year males are capable of breeding early, so their presence results in a sharp increase each spring in the number of available males for females that might opt to seek a different partner. Moreover, the addition of first-year males to males that have switched partners overwinter or whose partner died overwinter may alter the overall mean investment levels of available males: the results presented here suggest that these incoming males are disproportionately likely to have been reared by parents in partnerships that persisted across breeding attempts, and both parental provisioning behaviour (Dor & Lotem, 2010) and the number of recruits house sparrows produce annually (Schroeder et al., 2012) are heritable. The season effect could well result from a combination of all three factors: some partner switches may occur by chance, and the effects of attrition plus phenotypic plasticity may account for the remainder. Regardless, in terms of its potential to promote cooperation, these results indicate that when a shifting threshold remains sensitive to breeding outcome and peak switching coincides with increased selective incentives for remaining paired with the same partner, it can perform qualitatively similarly to a process in which the optimal threshold co-evolves with the mean cooperative effort level (McNamara et al., 2008). More generally, although house sparrows deviate in several respects from the assumptions of McNamara et al.’s (2008) model, these results demonstrate the feasibility of the process they outlined for the evolution of increased levels of cooperative investment. Partner switching, like sanctioning, requires that an organism responds to some aspect of its experiences with a collaborator (Foster & Wenseleers, 2006). Theoreticians portray the nature of these responses in various ways. Most discussions of partner switching describe dismissal as being contingent on either the actions of the partner or inferences about partner

action based on the interaction’s outcome (No€ e & Hammerstein, 1995; Sachs et al., 2004; McNamara et al., 2008; Izquierdo et al., 2010). Alternatively, partner switching may simply be contingent on outcomes. Low breeding success precedes partner switching in multiple avian species (Ens et al., 1996; Dubois & Cezilly, 2002), and this poor breeding success, in turn, has been found to correlate with deficiencies in partner parental care (Moody et al., 2005) or breeding site quality (e.g. Desrochers & Magrath, 1993; Garcıa-Navas & Sanz, 2011). But whether the birds actually rely on information about partner behaviour (or partner-controlled resources) as their criterion for switching, or whether they respond to outcomes, is not known. The issue of how specifically the criterion for partner switching targets uncooperative partners parallels the distinction in the mutualism literature between host sanctions and partner fidelity feedback (Weyl et al., 2010; Archetti et al., 2011; see also Leimar & Hammerstein, 2010). Both sanctions and partner fidelity feedback can result in fitness reductions for uncooperative symbionts, and experimental manipulations are required to discriminate between the two (Weyl et al., 2010; Archetti et al., 2011). But as Archetti et al. (2011) note, regardless of whether host responses are ‘actionbased’ or ‘outcome-based’, selection will still promote symbiont cooperation if uncooperative symbionts have reduced fitness; the chief difference is whether the host response evolved in the context of the mutualism. Given that male house sparrows reproduce poorly when they switch partners, selection will favour male cooperative investment so long as higher investment places males at lower risk of a partner switch. Overwintering pairs, in particular, cannot achieve the high breeding outcomes that are associated with a low risk of switching without substantial male investment. Females of this species do not adjust their provisioning behaviour in response to reduced contributions by their mates (Schwagmeyer et al., 2002; Mazuc et al., 2003), and as a result, experimentally induced reductions in male parental care negatively affect multiple components of breeding success (Mazuc et al., 2003; Schwagmeyer et al., 2012). Testosterone manipulation, for example, reduces male feeding rates by 50% or more (Hegner & Wingfield, 1987; Mazuc et al., 2003; Schwagmeyer et al., 2005). Based on the results here (Appendix S1, D2), the mean breeding outcomes of treated males (from table 1, Schwagmeyer et al., 2012) would place them at about a 60% chance of an overwinter switch. It seems doubtful, though, that the basic behaviours involved in sparrow partner switching (the independent movement of one or both pair members to a different nesting site) evolved in the context of biparental investment. For instance, female house sparrows that are disturbed while laying eggs or incubating are highly likely to desert their nesting site (Seel, 1968), which often equates with desertion of their partner.



This is presumably a reaction to perceived predation risk, and for first-time partners, it occurs prior to the expression of much male parental care. Nevertheless, so long as perceived predation risk is typically independent of or negatively correlated with male cooperative investment, partner switching will still favour males that invest at higher levels.

Acknowledgments I thank David Queller, two anonymous reviewers and Andy Gardner for comments on the manuscript, and Jennifer Alig, Terri Bartlett, Matt Dugas, Christine Edly-Wright, Amy Kopisch, Bonnie Means, Doug Mock, Lace Svec, Taryn West and Lindsay White for their efforts at the North Base study site during the years of this study. This research was supported by National Science Foundation Grants IBN 9982661 and IOS 0843673.

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Supporting information Additional Supporting Information may be found in the online version of this article: Appendix S1 (A–E) Additional details on methods and results. Data deposited at Dryad: doi:10.5061/dryad.7mv2b Received 18 April 2014; revised 2 July 2014; accepted 4 July 2014


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