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Evolution of sex differences in cooperation can be explained by trade-offs with dispersal [1]

['Pablo Capilla-Lasheras', 'Centre For Ecology', 'Conservation', 'University Of Exeter', 'Penryn', 'United Kingdom', 'Swiss Ornithological Institute', 'Bird Migration Unit', 'Sempach', 'School Of Biodiversity']

Date: 2024-10

Explaining the evolution of sex differences in cooperation remains a major challenge. Comparative studies highlight that offspring of the more philopatric sex tend to be more cooperative within their family groups than those of the more dispersive sex but we do not understand why. The leading “Philopatry hypothesis” proposes that the more philopatric sex cooperates more because their higher likelihood of natal breeding increases the direct fitness benefits of natal cooperation. However, the “Dispersal trade-off hypothesis” proposes that the more dispersive sex cooperates less because preparations for dispersal, such as extra-territorial prospecting, trade-off against natal cooperation. Here, we test both hypotheses in cooperatively breeding white-browed sparrow weavers (Plocepasser mahali), using a novel high-resolution automated radio-tracking method. First, we show that males are the more dispersive sex (a rare reversal of the typical avian sex difference in dispersal) and that, consistent with the predictions of both hypotheses, females contribute substantially more than males to cooperative care while within the natal group. However, the Philopatry hypothesis cannot readily explain this female-biased cooperation, as females are not more likely than males to breed within their natal group. Instead, our radio-tracking findings support the Dispersal trade-off hypothesis: males conduct pre-dispersal extra-territorial prospecting forays at higher rates than females and prospecting appears to trade-off against natal cooperation. Our findings thus highlight that the evolution of sex differences in cooperation could be widely attributable to trade-offs between cooperation and dispersal; a potentially general explanation that does not demand that cooperation yields direct fitness benefits.

First, we demonstrate that the sex differences in dispersal and cooperation in sparrow-weaver societies satisfy the predictions of both the Philopatry and Dispersal trade-off hypotheses: This species shows a reversal of the typical avian sex biases in both dispersal incidence and natal cooperation. We then test for the underlying processes assumed by the Philopatry and Dispersal trade-off hypotheses to establish whether either hypothesis can explain why this rare example of female-biased Philopatry in birds is accompanied by female-biased natal cooperation. Regarding the Philopatry hypothesis, we test whether female helpers are indeed more likely than males to inherit the breeding position within their natal group; the commonly invoked mechanism by which the more philopatric sex could gain a greater downstream direct benefit from cooperation [ 1 , 3 ]. Regarding the Dispersal trade-off hypothesis, we use a high-resolution automated radio-tracking study of extra-territorial prospecting to test its two key assumptions: first, that male helpers (the more dispersive sex) prospect at higher rates or over greater distances or for longer durations than females; second, that investments in prospecting from the natal group trade-off against concurrent investments in natal cooperative care.

Subordinate female sparrow-weavers cooperatively feed offspring at substantially higher rates than subordinate males [ 19 ], a pattern rarely documented among birds [ 5 ]. Here, we demonstrate that this marked sex difference in cooperation is evident among subordinates within their natal groups, in the absence of a sex difference in relatedness to recipients (see Results for both findings). Helper contributions are known to increase the overall rates at which nestlings are fed [ 19 ]. This appears to increase offspring survival to fledging in dry conditions but actually reduce it in wet conditions [ 19 ], such that helping reduces the rainfall-induced variance in offspring survival to fledging (which may yield indirect fitness benefits via mechanisms such as altruistic bet-hedging; [ 19 ]) without impacting the mean level of offspring survival to fledging once one integrates across environmental conditions [ 19 ]. Helping may also yield indirect fitness benefits by lightening the workloads of related breeders [ 26 , 27 ], thereby improving the survivorship of the dominant female [ 28 ] and allowing her to invest more per offspring at the egg stage when helped [ 29 ]. The combined effects of helping on maternal investment at the egg stage and the total rate of nestling provisioning could also yield indirect fitness benefits by improving offspring quality [ 26 ] but this remains to be tested. Helping could also conceivably yield direct fitness benefits, but as subordinate immigrants rarely help at all [ 27 ], it seems unlikely that these benefits are substantial (see Discussion for more detail). Helping behaviour could, for example, yield a downstream direct fitness benefit to helpers if they inherited the dominant (breeding) position in their natal group and were then helped by offspring that they had previously helped to rear; the mechanism commonly envisaged in the Philopatry hypothesis [ 3 , 6 ].

Here, we combine long-term data on life-histories and cooperative behaviour with a high-resolution automated radio-tracking study of prospecting to test both the predictions and core assumptions of the Philopatry and Dispersal trade-off hypotheses, using wild cooperatively breeding white-browed sparrow weavers, Plocepasser mahali, as a model system. White-browed sparrow weavers (hereafter “sparrow weavers”) are cooperative birds that live in social groups and defend year-round territories across the semi-arid regions of sub-Saharan Africa. Within each group, a single dominant male and female monopolise reproduction and their offspring of both sexes delay dispersal, becoming nonbreeding subordinates (occurring at an approximately even sex ratio; [ 19 ]) that cooperatively help to feed future generations of nestlings produced by the breeding pair [ 20 ]. As offspring of both sexes never breed while subordinate [ 20 ], the only route to natal breeding is via inheritance of the natal dominant (breeding) position. The primary route to dominance for both sexes, however, is via dispersal to other groups [ 21 ], which may offer immediate access to vacant dominant positions and is likely to reduce the risk of inbreeding [ 20 , 22 , 23 ]. Dispersal is typically local in both sexes but genetic analyses and field observations suggest that males disperse further than females from their natal to breeding sites and thus that females may be the more philopatric sex [ 21 ], a rare reversal of the typical passerine sex-bias in dispersal [ 24 ]. Here, we establish whether there are also clear sex biases in dispersal incidence and natal breeding position inheritance, the dispersal traits most relevant to the rationale of the focal hypotheses. Subordinates of both sexes conduct extra-territorial prospecting forays prior to dispersal from their natal group, which are commonly met with aggression from territory holders [ 21 , 25 ]. The rarity of extra-group parentage by subordinates (<1% of paternity [ 20 ]) suggests that the primary function of these forays is to promote dispersal.

The Dispersal trade-off hypothesis proposes that offspring of the more dispersive sex help at lower rates (while both sexes reside within the natal group) because all individuals face a trade-off between investments in natal cooperation and activities that promote dispersal from the natal group, such as extra-territorial prospecting for dispersal opportunities [ 5 , 9 ]. Thus, while the Philopatry hypothesis requires that cooperation yields a downstream direct fitness benefit, the Dispersal trade-off hypothesis does not. In many social species, individuals prepare for dispersal by conducting extra-territorial prospecting forays from their natal group, which are thought to yield information on dispersal opportunities in the surrounding population [ 5 , 6 , 9 , 11 – 14 ]. Investments in prospecting could trade-off against natal cooperation because the two activities cannot be carried out at the same time and because costs and physiological changes associated with prospecting could reduce the expression of helping [ 9 , 12 , 14 – 16 ]. Frequent prospectors could also reduce their costly contributions to helping in order to maintain competitive phenotypes that reduce the risks and/or increase the likely success of prospecting [ 17 ]. However, little is known about prospecting due to the difficulty of monitoring the cryptic, fast, and often long-distance movements that prospectors make [ 5 , 9 , 11 , 13 , 15 ]. One study of male meerkats, Suricata suricatta, whose frequent extra-territorial forays yield extra-group matings [ 18 ], suggests that investments in such forays may indeed trade-off against cooperation [ 9 ]. But whether prospecting for dispersal opportunities per se (which may occur at lower rates than mating forays and could entail different costs) can also trade-off against natal cooperation, as envisaged under the Dispersal trade-off hypothesis, is not yet known.

The leading hypothesis for the evolution of sex differences in natal cooperation, the “Philopatry hypothesis,” proposes that offspring of the more philopatric sex help at higher rates (while both sexes reside within the natal group) because, by staying in their natal group for longer they stand to gain a greater direct fitness benefit from cooperation [ 1 , 3 , 6 ]. This hypothesis therefore requires that cooperation yields a direct fitness benefit and that the accrual of this benefit is to some extent contingent upon remaining within the natal group. For example, the more philopatric sex may be more likely to ultimately breed within the natal territory and may thus stand to gain a greater downstream direct benefit from cooperating to rear additional group members that may ultimately help them in the future [ 1 – 3 , 6 ]. A recent comparative study of the cooperative birds in which both sexes delay dispersal and help has found support for this idea [ 3 ]; species with more female-biased probabilities of natal breeding showed more female-biased helper contributions to cooperative care while within the natal group. These findings are consistent with the key prediction of the Philopatry hypothesis and could therefore constitute rare evidence that direct fitness benefits have played a widespread role in the evolution of helping [ 3 , 10 ]. However, these findings are also consistent with an alternative less-studied hypothesis which also predicts that the more philopatric sex should help more, regardless of whether helping yields a direct benefit, the “Dispersal trade-off hypothesis.”

The evolution of sex differences in cooperation remains a major evolutionary puzzle [ 1 – 6 ]. In many cooperatively breeding species, in which offspring of both sexes delay dispersal from their natal group and help to rear future generations of their parents’ young, one sex contributes significantly more than the other to cooperative care within the natal group ([ 1 , 3 – 5 , 7 , 8 ]; see also [ 3 , 4 ] for exceptions). These sex differences in natal cooperation are of particular interest as they occur in the absence of sex differences in relatedness to recipients (as helpers of both sexes are still residing within their natal groups), leaving it unlikely that kin selection alone can explain their evolution [ 1 , 3 – 6 ]. Recent comparative analyses have highlighted that, across cooperative breeders of this kind, sex differences in contributions to cooperative care while within the natal group are predicted by the species’ sex difference in dispersal: resident offspring of the more philopatric sex tend to contribute more to natal cooperation than resident offspring of the more dispersive sex [ 3 , 4 ]. However, it is not clear why the more philopatric sex contributes more to natal cooperation, as the two major evolutionary explanations proposed for this pattern have not been teased apart [ 1 , 3 – 5 , 9 ].

( A ) A subordinate female (females have pale bills) fitted with an Encounternet radio-tag (pictured inset). The tag is fitted with leg loops and sits on the bird’s lower back. The aerial can be seen sitting along the tail feathers. ( B ) Circadian variation in prospecting behaviour; mean hourly prospecting rates per bird per hour of the day (mean ± SE; from the 27 radio-tracked birds). The shaded area illustrates night hours (using the local civil twilight time on March 11, 2017, the middle date of our tracking study). The rare forays at night could reflect birds being flushed from their roost chambers by predators. We found no evidence of sex differences in either the ( C ) mean duration of forays ( S7 Table ) or ( D ) mean estimated round-trip distance travelled on forays ( S8 Table ). ( E ) Subordinate males have a significantly higher daily prospecting rate than subordinate females, both inside and outside peak periods of cooperative nestling provisioning ( S6 Table ). ( F ) Individual variation in prospecting rate negatively predicted cooperative provisioning rate for the 13 radio-tagged birds with prospecting data during a nestling provisioning period ( S9 Table ; the plot shows >13 data points as we have repeated measures per individual). Male and female model estimates in C , D , and E illustrated in green and purple colour, respectively. C , D , E , and F present mean model predictions ± SE. Data and code needed to generate this figure can be found at https://doi.org/10.5281/zenodo.13623047 .

Consistent with our direct observations above, subordinate males showed significantly higher daily rates of prospecting from their natal groups than subordinate females (χ 2 1 = 5.39, p = 0.020; Fig 3E and S6 Table ). Prospecting rates were modestly but not significantly lower during nestling provisioning periods (i.e., when cooperative care occurs) than at other times (χ 2 1 = 2.15, p = 0.142; Fig 3E and S6 Table ). The magnitude of the sex difference in prospecting rate was not affected by whether the bird’s social group was provisioning nestlings at the time (χ 2 1 = 0.97, p = 0.324; S6 Table legend). There was no evidence of an effect of subordinate sex or nestling provisioning periods on either the duration (both χ 2 1 < 0.09, p > 0.77; Fig 3C and S7 Table ) or estimated distance of forays (both χ 2 1 < 0.80, p > 0.37; Fig 3D and S8 Table ). Older subordinates conducted forays of shorter duration (χ 2 1 = 3.95, p = 0.047; S7 Table ) but age did not predict prospecting rate (χ 2 1 = 0.23, p = 0.631; S6 Table ) or distance (χ 2 1 = 0.14, p = 0.708; S8 Table ). Focussing on the subset of radio-tagged subordinates whose forays were tracked through a nestling provisioning period, we also found evidence suggestive of a trade-off between prospecting and cooperative provisioning. Despite the modest sample size available for this analysis (34 daily measures of provisioning rate with matched prospecting effort data, from 13 subordinates across 7 social groups), an individual’s prospecting rate over the three-day window prior to us quantifying cooperative contributions to nestling provisioning significantly negatively predicted its cooperative provisioning rate (χ 2 1 = 5.08, p = 0.024; Fig 3F and S9 Table ). The existence of this negative correlation between prospecting and cooperative provisioning rate was also robust to the choice of time window over which we calculated prospecting effort ( S2 Fig ).

We deployed an automated radio-tracking technology to provide continuous high-resolution information on the prospecting movements of 27 radio-tagged subordinate adults residing within their natal groups (13 males and 14 females, Fig 3A ). After processing the 22,518,022 detection logs from the base station receiver array (see Methods ), we detected a total of 971 extra-territorial prospecting forays. We used a conservative approach to identify forays (see Methods ): events in which the signal-strength distribution across the receiver array suggested that the bird’s closest base-station was >250 m away from the centre of their own territory (where there was also always a base-station). As base-stations were situated in the centres of all territories within the tracking study area and the mean ± SE distance between neighbouring territory centres was just 93.7 m ± 4.56 m, these events should typically constitute forays beyond the territory centres of neighbouring groups (see Methods ). This approach will minimise the chance that a resident bird’s territorial interactions with its neighbours are incorrectly interpreted as extra-territorial prospecting, but may underestimate foray frequency by excluding more local prospecting. These 971 forays principally occurred between 06:00 h and 19:00 h, with frequencies peaking in the cooler periods towards the start and end of the day ( Fig 3B ). The tagged bird’s estimated daily rates of prospecting varied widely from 0 to 26 forays per day (n = 895 daily rate measures from 27 tagged birds; mean = 1.09 forays/day; median = 1 foray/day). Forays had a mean duration of 18.59 min (median = 5.67 min; range = 0.42 to 493 min). Our best estimate of the round-trip distance travelled per foray had a mean of 720.74 m (median = 647.60 m; range = 502.29–2026.15 m), though this is likely an underestimate as our ability to detect longer-distance forays was constrained by the spatial coverage of our receiver array ( S1 Fig ), and as the estimate was calculated as twice the straight line distance to the bird’s furthest location (while the birds could have taken a more complex path).

Subordinate females (purple points; the more cooperative sex; Fig 1B ) were no more likely to inherit a natal breeding position than subordinate males (green points; S4 Table ). Our analyses focussed on subordinates within their natal group at a given focal age and tested for an effect of sex on their probability of inheriting natal dominance at some later time. The solid points show the sex-specific means (± SE) for the focal age class, and the translucent points represent raw data. Subordinates were only included in the analysis if dominance was monitored within their focal group for at least 2 years after the date on which the subordinate reached the focal age. Data and code needed to generate this figure can be found at https://doi.org/10.5281/zenodo.13623047 .

Contrary to expectations under the Philopatry hypothesis, females were no more likely than males to obtain a dominant breeding position within their natal group (χ 2 1 = 0.29, p = 0.592; Fig 2 and S4 Table ). For natal subordinates under 3 years of age, the probability of ultimately inheriting natal dominance was low (<10% on average, Fig 2 ) and showed no sex difference, yet sex differences in natal cooperation were clear at these ages ( Fig 1B ). Once subordinates reached 3 years of age within their natal group their probability of inheriting natal dominance markedly increased (to approximately 25%), but their contributions to natal cooperation markedly decreased ( Fig 1B ). If we also included in these “natal dominance acquisition” events any dominant breeding positions acquired outside the natal group by founding a new group within a territory previously held by the natal group (i.e., territorial budding [ 6 ]), we still found no evidence of a sex difference in the probability of natal dominant acquisition (χ 2 1 = 1.89, p = 0.169; S5 Table ). Overall, dominance turnover events rarely involved subordinates winning dominance within their natal group, and the sexes did not differ in this regard (just 7 natal dominance wins of 32 total turnovers for males; 9 natal of 32 total for females; χ 2 1 = 0.08, p = 0.773); dominance was typically acquired in both sexes via dispersal to other groups. The observed male-bias in age-specific dispersal probability ( Fig 1A ) appears, therefore, to reflect a sex difference in the strategy used to acquire dominance via dispersal, rather than in the incidence of acquiring dominance via dispersal (see Text D in S1 File ).

Subordinate females did indeed feed broods at significantly higher rates than subordinate males while within the natal group (χ 2 1 = 16.69, p < 0.001; Fig 1B and Table 2 ). The provisioning rates of subordinates also increased initially with advancing age before decreasing slightly ( Fig 1B ; age effect: χ 2 3 = 27.41, p < 0.001; Table 2 ). There was no indication that the magnitude of the sex difference in cooperation changed significantly with age (χ 2 3 = 5.41, p = 0.162; Table 2 ). Brood size and brood age both positively predicted subordinate provisioning rates (both χ 2 1 > 11.50, p < 0.001; Table 2 ). During their provisioning visits, subordinate females also spent slightly but significantly longer than subordinate males within the nest chamber (χ 2 1 = 16.46, p < 0.001; Fig 1C and S1 Table ) and were just as likely as subordinate males to provision nestlings with food items that were large (χ 2 1 = 1.43, p = 0.231; Fig 1D and S2 Table ). These sex differences in the provisioning rates of subordinates within the natal group occurred in the absence of sex differences in their relatedness to the nestlings being fed (χ 2 1 = 0.16, p = 0.691; Fig 1E and S3 Table ).

Among subordinate birds residing within their natal groups, ( A ) males (green points) showed significantly higher age-specific probabilities of dispersal than females (purple points; Table 1 ), while ( B ) females showed significantly higher cooperative nestling provisioning rates than males (a sex difference that did not vary with age; Table 2 ). ( C ) Natal subordinate females also spent slightly but significantly longer in the nest per provisioning visit than males ( S1 Table ) and ( D ) were just as likely as natal subordinate males to feed the nestlings with food items that were large ( S2 Table ). ( E ) These sex differences in natal cooperation occurred in the absence of a sex difference in relatedness to the nestlings being fed ( S3 Table ). Translucent points represent raw data whereas larger points and error bars give mean model predictions ± SE (where error bars cannot be seen, they are smaller than the radius of the point presenting the mean). Data and code needed to generate this figure can be found at https://doi.org/10.5281/zenodo.13623047 .

Consistent with the predictions of both hypotheses, sparrow weavers show a significant male-bias in dispersal incidence coupled with a significant female-bias in contributions to natal cooperation. Modelling the age-specific probability of dispersal from the natal group revealed that subordinate natal males are significantly more likely to disperse than subordinate natal females across all age classes (χ 2 1 = 9.64, p = 0.002; Fig 1A and Table 1 ). There was also evidence that dispersal probability increased with age (χ 2 3 = 64.98, p < 0.001; Fig 1A and Table 1 ), but no evidence that the sex difference in dispersal probability changed with age (χ 2 3 = 1.35, p = 0.717; Table 1 ). The Philopatry and Dispersal trade-off hypotheses would therefore both predict that subordinate females (the more philopatric sex) should help at higher rates than subordinate males (the more dispersive sex) while within the natal group.

Discussion

Our findings reveal that white-browed sparrow weavers show a rare reversal of the typical avian sex difference in dispersal: males show higher age-specific probabilities of dispersal from their natal group than females and both population genetics and observed dispersals suggest that males disperse further than females from their natal to breeding sites [21]. Undetected longer-distance dispersals (beyond the bounds of our study site) may also be more common among males, as the low rate of immigration into our study population is also male biased [21]. Both the Philopatry and Dispersal trade-off hypotheses for the evolution of sex differences in cooperation would therefore predict that sparrow-weavers show female-biased natal cooperation, and our findings confirm this. Natal subordinate females helped to feed nestlings at higher rates than natal subordinate males across the age classes, and spent longer within the nest on their visits. This coupling of reversals of the typical avian sex biases in both dispersal and cooperation provides novel support for the predictions of the focal hypotheses, which are otherwise difficult to test given the limited variation in dispersal sex biases within taxonomic classes [3–5]. While our finding of female-biased natal cooperation is unusual for cooperative birds, this is principally the case because in many cooperative bird species only males delay dispersal and so only males are available to help within the natal group [2]. Among those cooperative bird species in which both sexes delay dispersal from their natal group and help, significantly female-biased rates of helping with one or more forms of care while within the natal group now appear to have been documented in a comparable number of species to significantly male-biased rates of helping [4]. Below, we consider the potential for the Philopatry and Dispersal trade-off hypotheses to account for the evolution of female-biased natal cooperation in this species, drawing on our empirical tests of the underlying mechanisms assumed by each. Our findings suggest that the mechanisms envisaged in the Philopatry hypothesis are unlikely to be acting in this species, and that the evolution of female-biased cooperation can be more readily explained by the Dispersal trade-off hypothesis. We consider the wider implications of this finding for our understanding of the evolution of sex differences in cooperation and, more broadly, the role that direct benefits of helping have played in the evolution of cooperation across taxa.

Among the diverse hypotheses proposed for the evolution of sex differences in cooperation [2,4], the Philopatry and Dispersal trade-off hypotheses are unusual in predicting the evolution of female-biased natal cooperation in sparrow-weaver societies; alternative hypotheses cannot readily explain this pattern. That the observed sex difference in natal cooperation occurs in the absence of a sex difference in average relatedness to recipients suggests that it cannot be attributed to a sex difference in the indirect benefits of cooperation [1,3,4]. While the indirect benefits of cooperation are also a product of the effect of a given unit of cooperation (e.g., a given provisioned food item here) upon the fitness of the recipient (b in Hamilton’s rule; [30]), it is not likely that sex differences exist in this; items of provisioned food are expected to impact the fitness of recipients regardless of the sex of donor. The heterogamety hypothesis [2,4,31] proposes that effects of the sex chromosomes on patterns of genetic relatedness could leave the heterogametic sex (females in birds) less cooperative, yet we see the opposite pattern here. Similarly, the paternity uncertainty hypothesis [2,4,32] predicts male-biased cooperation when extra-pair paternity occurs, yet we see the opposite pattern here despite dominant males losing 12% to 18% of paternity to other (i.e., extra-group) dominant males [20]. The parental skills hypothesis [2,4] proposes that the sex that invests most in parental care could contribute most to helping if (i) helping yields a direct benefit by improving parenting skills; and (ii) this benefit is larger for the sex that contributes most to parental care. This hypothesis could be relevant to sparrow-weavers as dominant females feed offspring at higher rates than dominant males [27]. However, compelling evidence that helping improves parenting skills remains elusive [2,33], and as immigrant subordinate sparrow-weavers rarely help at all [27], it seems unlikely that direct benefits arising via skills acquisition are a major driver of helping in this system. It has also been suggested that the sex that shows higher variance in lifetime reproductive success (LRS) may invest more in helping given its lower chance of securing direct fitness by breeding [2,34]. However, male and female sparrow-weavers likely have very similar variances in LRS, as both sexes only breed as dominants and do so in socially monogamous pairs [20] with no evident sex difference in dominance tenure length (t = −0.25, df = 62, p = 0.800, n = 32 male tenures, 32 female tenures, means ± SE: males = 2.62 ± 0.32 years, females = 2.51 ± 0.33 years). If anything, competition for extra-group paternity among dominant males [22] may leave males with slightly higher variance in LRS than females, but this would lead to the prediction of male-biased natal cooperation, and we observe the reverse. It is also unlikely that female helpers cooperatively provision more because male helpers contribute more to other cooperative activities (i.e., a sex-based division of cooperative labour) because female helpers contribute just as much as males to cooperative sentinelling and territory defence [25,35]. As helping may improve the survival of the dominant female [28] (by lightening her provisioning workload [29]), another possibility is that a sex difference exists in the direct cost to subordinates of helping to do so. For example, the survival of the dominant female is a direct barrier to the subordinate female inheriting the dominant breeding position and so subordinate females may pay a greater direct cost of helping via this mechanism (particularly as they may on average stay for longer in their natal groups than males; Fig 1A). However, this would lead to the expectation that subordinate females contribute less (rather than more) to cooperative care. It also is not clear that a sex difference in this cost exists, as subordinate males could face a similar direct cost of prolonging dominant female survival (as a son becoming a natal breeding dominant might also be contingent upon the death of their mother if she avoids close inbreeding [23]).

The Philopatry hypothesis proposes that offspring of the more philopatric sex contribute more to natal cooperation because, by staying in their natal group for longer, they stand to gain a greater downstream direct benefit from natal cooperation [1,3,6]. The commonly invoked mechanism by which the more philopatric sex could gain a greater direct benefit from cooperation is if they were more likely to ultimately breed in their natal group and thus benefit from having helped to increase the size of the natal workforce [1,3,6]. This mechanism cannot readily explain female-biased natal cooperation in sparrow weavers, as neither sex breeds within their natal group while subordinate [20], and our findings suggest that subordinate females are no more likely than males to inherit a dominant breeding position within their natal territory. Indeed, our findings also give cause to question whether helping in this species yields any form of direct benefit contingent upon inheriting natal dominance. If it did, one might expect the markedly higher chance of inheriting natal dominance beyond 3 years old (Fig 2) to be accompanied by a concomitant increase in natal cooperation, yet we observe the opposite (Fig 1B). This pattern may instead reflect subordinates showing greater restraint from costly helping once they become credible contenders for dominance [36]. A second mechanism by which the more philopatric sex might gain a greater downstream direct benefit from natal helping, regardless of whether they inherit natal dominance, is if (i) helping to rear offspring augments natal group size; and (ii) living in a larger natal group then improves survival. However, this mechanism is also unlikely to apply in sparrow-weavers as (i) helping does not appear to augment group size (as helper numbers do not positively predict the mean rate of offspring survival or the breeding rate of dominant females [19]); and (ii) subordinate sparrow weavers appear to suffer markedly lower survival rates in larger social groups, suggesting that group augmentation would actually yield direct fitness costs rather than benefits [28]. Indeed, it seems unlikely that helping yields an appreciable direct benefit of any kind in sparrow weaver societies (e.g., via other mechanisms such as “pay to stay” or signalling “quality” [37–40]), as subordinates rarely contribute to cooperative care following dispersal from their family groups [20,27]. Together, our findings suggest that the Philopatry hypothesis cannot readily account for the evolution of female-biased natal cooperation in this species.

The Dispersal trade-off hypothesis proposes that the more dispersive sex contributes less to natal cooperation because all individuals face a trade-off between activities that promote dispersal (such as prospecting for dispersal opportunities) and natal cooperation [5,9]. It thus envisages that sex differences in cooperation arise not from a sex difference in the direct benefits of cooperation but from a trade-off between cooperation and other fitness-relevant traits in which sex differences exist. Our findings support the key prediction of this hypothesis, that male-biased dispersal should be accompanied by female-biased natal cooperation, and provide evidence in support of the underlying mechanisms that it envisages. First, our automated radio-tracking study revealed that natal subordinates of both sexes prospect, but males (the more dispersive sex) prospect at significantly higher rates than females, while making forays of comparable duration and distance. Our direct observations of prospectors visiting our study groups also reflect this male-bias in prospecting incidence. Subordinate males may benefit more from prospecting than females because they are more likely than females to disperse in all age classes, and because they disperse further on average than females between their natal and breeding sites [21]. While forays in some species function in extra-group mating [18,41,42], the forays of subordinate sparrow-weavers do not appear to serve this purpose as both within- and extra-group paternity are monopolised by dominant males [20,22]. That this male bias in prospecting was apparent during nestling provisioning periods highlights its potential to drive sex differences in cooperative care. That the sex difference in prospecting was also apparent outside nestling provisioning periods suggests that it is unlikely to be a product of the sex difference in natal cooperation (i.e., a reversal of the causal direction suggested above), as it also occurs when subordinates are not engaged in cooperative care.

Our automated radio-tracking study also revealed support for the second key assumption of the Dispersal trade-off hypothesis: that investments in prospecting trade-off against investments in cooperative care. Despite the modest sample size available, our analysis revealed that individual variation in prospecting rate significantly negatively predicts cooperative provisioning rate, consistent with the expectation of a trade-off between the two. Thus male and female sparrow weavers may differ in their mean contributions to cooperative care because they differ in their mean prospecting rate and the two traits are subject to a trade-off (the rationale of the Dispersal trade-off hypothesis). As prospecting and cooperative care are both likely to entail energetic costs [9,12,17] and are mutually exclusive activities (feeding within the natal territory cannot occur while prospecting elsewhere), the observed negative association between the two traits could reflect a simple resource and/or time allocation trade-off (potentially mediated by endocrine changes associated with prospecting [9,42]). While forays could well entail intense energetic expenditures and will reduce the time available for feeding, the total energetic and/or time cost of prospecting in this species need not necessarily be high, as the detected forays occurred on average at modest daily rates (though our analyses could underestimate this) and were often short in duration. However, prospecting is also likely to entail a significant risk of injury and death, due to attacks by conspecifics [5,9,12,13] and predators [15]. As such, regular prospectors may benefit more than others from maintaining a competitive phenotype (to mitigate the risk of injury and enhance dispersal success), which could itself trade-off against investments in cooperation, compounding the effects of any energetic and/or time costs entailed in prospecting. As both of these trade-off mechanisms are consistent with the rationale of the Dispersal trade-off hypothesis, this hypothesis seems well placed to explain the evolution of female-biased natal cooperation in this species: males contribute less to natal cooperation because male-biased dispersal leaves them prospecting more, and all individuals face a trade-off between prospecting and natal cooperation.

Our study has tested the predictions and assumptions of the Philopatry and Dispersal trade-off hypotheses for the evolution of sex differences in cooperation. Our findings suggest that the mechanisms envisaged in the Dispersal trade-off hypothesis are better placed to explain the evolution of female-biased natal helping in sparrow-weaver societies than those envisaged in the Philopatry hypothesis. This is important because the Philopatry hypothesis is commonly invoked as the likely driver of the association between sex differences in Philopatry and cooperation across taxa (e.g., [1,3,4]), but the Dispersal trade-off hypothesis also predicts this pattern [4,5,9]. Moreover, the Dispersal trade-off hypothesis could apply more widely across taxa, as it does not require that helping yields a direct fitness benefit contingent upon remaining in the natal group, a scenario whose generality is unclear. The mechanisms envisaged in the Philopatry hypothesis could certainly apply in some species, such as those in which helping augments group size and in which group augmentation could yield a downstream direct benefit to helpers (e.g., Florida scrub jays, Aphelocoma coerulescens [6] and meerkats [1]). Indeed, the mechanisms envisaged in both hypotheses could act in concert to select for sex differences in helping in such species (e.g., both Florida scrub jays and meerkats also show sex differences in helper prospecting [6,9,18]). Our findings highlight the need for caution, however, when extrapolating the Philopatry hypothesis to species in which helping may not yield direct benefits or in which mechanisms for the differential downstream accrual of such benefits by the more philopatric sex have not been identified. On balance, it seems likely that the mechanisms envisaged in the Philopatry and Dispersal trade-off hypotheses have both played a role in the evolution of sex differences in natal cooperation, but their relative importance may vary markedly among species.

Our findings have wider implications too for the role that direct benefits of helping may have played in the evolution of cooperation. Recent comparative studies have highlighted that the probability that helpers will breed within their natal group predicts helper contributions to cooperative care across taxa [3,10], and it has been suggested that these findings constitute rare evidence that direct fitness benefits of helping have played a widespread role in the evolution of helping, alongside kin selection [3,4,10]. However, our findings suggest that such associations could also arise in the absence of direct benefits of helping, via trade-offs between dispersal and cooperation: helpers with higher probabilities of natal breeding might generally contribute more to natal cooperation across taxa because they need not invest as much in preparations for dispersal. Thus, while direct benefits of helping may indeed be important in some contexts (e.g., [1,39,40]), how widespread a role they have played in the evolution of helping behaviour across taxa would seem to remain an open question.

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[1] Url: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3002859

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