In most species, males do not abandon offspring or reduce paternal care when they are cuckolded by other males. This apparent lack of adjustment of paternal investment with the likelihood of paternity presents a potential challenge to our understanding of what drives selection for paternal care. In a comparative analysis across birds, fish, mammals, and insects we identify key factors that explain why cuckolded males in many species do not reduce paternal care. Specifically, we show that cuckolded males only reduce paternal investment if both the costs of caring are relatively high and there is a high risk of cuckoldry. Under these circumstances, selection is expected to favour males that reduce paternal effort in response to cuckoldry. In many species, however, these conditions are not satisfied and tolerant males have outcompeted males that abandon young.
Parental care is demanding: the effort it takes a typical garden bird to raise a clutch of chicks to adulthood is equivalent, in human terms, to cycling the Tour de France [1]. Intuition suggests that a male should only embark on this feat if he is the father of the chicks in his nest—if he has been cuckolded, he should avoid wasting resources on enhancing the reproductive success of his rivals and reduce paternal effort. Forty years of empirical research, however, have failed to provide consistent support for this prediction [2]. While there are exceptions, in the majority of species, it is reported that males do not significantly decrease care when cuckolded [2]–[5], challenging our understanding of how natural selection favours males that provide parental care. If information about paternity is unavailable or unreliable, selection may favour males that continue to provide care to avoid potential costs of abandoning their own offspring [6], [7]. Consequently, attempts to test explanations for the lack of paternal care adjustment have focussed on the ability of males to accurately assess paternity, but this has yielded abundant unexplained variation between species [2]. Another explanation is that variation in adjustment reflects differences in the strength of selection on males to reduce paternal care in response to loss of paternity. Firstly, theory predicts that the behaviour of males should optimise lifetime reproductive success rather than just paternity [8], [9]. This is formalised in Hamilton' s Rule, rb−c>0, where r is the relatedness between the caring male and offspring in this context, b is the fitness benefit of care to offspring, and c is the cost of care to future reproductive success of the male [10]. Cuckolded males are, therefore, predicted to be relatively tolerant of cuckoldry if paternal care does not reduce future reproductive success (low c) [8], [11], [12], and/or paternal care has little effect on offspring fitness (low b) [10], [13]. When b is low, variation in r has relatively weak effect on variation in selection (if we substitute b = 0 into rb−c>0, rb is always 0; if we substitute b = 1 into rb−c>0, rb varies from −1 to 1 depending on the value of r). Secondly, when there is little variation in the risk of cuckoldry between breeding attempts, or cuckoldry is rare, there will be weak selection for adjustment [11]. This is because rare or low variation in cuckoldry within males reduces the opportunity for selection to favour individuals that adjust paternal care [14]. Despite well-developed predictions about when cuckolded males should reduce care, our understanding of this problem remains limited because empirical studies have focused on reporting the presence or absence of adjustment without further formal analyses of causation.
We conducted a series of comparative meta-analyses to characterise the evolution of paternal care adjustment across species. We first quantified the strength of adjustment by calculating a standardised effect size (Pearson' s correlation coefficient: r) from the statistics reported in 62 studies that measured the relationship between paternity and paternal care across 48 species of fish, insects, birds, and mammals. This effect size, rAdjust, is the correlation coefficient between paternal investment and paternity: positive values of rAdjust indicate that reductions in paternal care are associated with loss of paternity; a value of zero indicates that investment in paternal care is independent of paternity; and negative values indicate paternal effort decreases with higher paternity. In contrast to the prevailing consensus across empirical studies, we found that males show a significant reduction in paternal care in response to female promiscuity across species. We found that rAdjust was positive in 81% of species and was significantly greater than zero overall (rAdjust mean effect = 0. 35,95% credible interval (CI) = 0. 10–0. 68, p = 0. 02; Figure 1; Table 1), despite the fact that only 44% of studies in our dataset report a significant effect of paternity on paternal care (Table S1). The difference between our meta-analysis of the strength of adjustment and “vote-counting” of significant results, indicates that failure to detect weak effects (type II error) and large variation between studies (Table 1) may have contributed to an underestimate of the extent to which males respond to cuckoldry. We also found that experimental manipulation of a male' s certainty of paternity did not cause greater adjustment in paternal care compared to observational studies (Table 1). Furthermore, rAdjust was significantly greater than 0 across experimental and observational studies and across studies that had measured different cues and used different methodology (Table S6). Together these results suggest that the ability of females to conceal promiscuous mating from males has been overestimated and the reported failure of studies to detect male adjustment cannot solely be explained by inaccuracy of cues. In addition to the significant overall effect of paternity on paternal care, our analysis revealed high variation in the strength of adjustment among species (Figure 1; Table 1), even after accounting for the possible confounding effects of phylogenetic history and differences in methodology (Tables 1 and 6). We tested predictions a priori that males of some species have stronger paternal care adjustment than others because of differences in the costs and benefits of paternal care and the risk of cuckoldry. We estimated the cost of care (c) by calculating the effect size (Pearson' s correlation coefficient: r) of paternal investment in a current breeding attempt on the probability of success in future breeding attempts (rCost) from published test statistics (Table S2). A positive value of rCost indicates that the level of investment in care for offspring in a current breeding attempt results in a correlated reduction in future breeding success. We estimated the benefits of paternal care (b) by measuring both the effect size (Pearson' s correlation coefficient: r) of male care on offspring fitness (rBenefit) from published test statistics and by obtaining data on the proportion of parental feeding visits performed by males from the literature (Table S3). A positive value for rBenefit indicates that more paternal care results in higher offspring survival. Finally, we estimated variation in female promiscuity (r) from the proportion of broods containing offspring fathered by more than one male (Table S1). We found that cuckolded males are significantly more likely to provide care when both the cost to future reproductive success is relatively low and cuckoldry is relatively rare (interaction between multiple paternity and rCost explained 13% of variation in rAdjust across species (reduction in residual variation when interaction was included in model): parameter estimate (β) = 0. 11, CI = 0. 01–0. 22, p = 0. 02; Figures 2 and 3, Table 1). The importance of this interaction is evident from the fact that a failure to reduce care in response to cuckoldry may be favoured even in species with a high risk of cuckoldry if there is relatively little cost to future reproductive success (Figure 2). In this case, the advantage of saving resources from withholding care are less likely to outweigh the costs of abandoning a brood where the male may have achieved some paternity success. Conversely, males also continue to care where the costs to future reproductive success are relatively high if female promiscuity is rarely or never encountered (Figure 2). This is because selection will not have had the opportunity to equip males with the ability to detect loss of paternity accurately and/or respond appropriately. For most species, however, some degree of adjustment has been favoured (Figure 1) and our results suggest that this is because caring for current offspring is generally costly to future reproductive success (rCost is significantly above zero across species – rCost mean effect size and CI = 0. 26 [0. 02–0. 50], p = 0. 04; Table 1) and the chance of cuckoldry is sufficient to drive the evolution of a response. In contrast, we found no evidence that variation in the benefit of paternal care on offspring fitness explains differences between species in adjustment. Males were no more likely to adjust in species with high rBenefit relative to species with low rBenefit (mean effect and CI = −0. 03 [−0. 12 to 0. 07, p = 0. 57; Table 1) and males that provided a greater proportion of total parental care were not more sensitive to paternity (mean effect and CI = −0. 003 [−0. 15 to 0. 16], p = 0. 95; Table S7). The effect of male care on offspring survival is relatively high across species (mean rBenefit = 0. 47 (−0. 27 to 0. 87; Table 1) and we speculate that within biparental or male-only care systems the effect of male care may be difficult to detect and measure (Table S4; Text S1). For example, the effect of male desertion is often not documented if offspring always die without male care. The data we collected on rAdjust comes from studies that measured the relationship between paternal care and paternity certainty both within and across males. It is therefore possible that our results are not only due to facultative adjustment of care, but also intrinsic differences between males. For example, a positive relationship between paternity and paternal care (positive rAdjust) may arise because poor quality males care less and are more often cuckolded [15], or because individual males adjust care in response to perceived paternity. To examine this possibility, we tested if our results differed according to whether rAdjust was measured across males or within males across breeding attempts. Values of rAdjust were significantly higher when changes within males were examined (Table 1), but the effect of rCost and rates of cuckoldry on rAdjust were consistent across studies using between and within subject designs (Table S7 (i) ). Furthermore, estimates of rAdjust were highly positively correlated across species where the relationship between paternity and paternal care had been measured both across and within males (Spearman' s Rank Correlation: Rs = 1. 00, n = 4, p<0. 001, Pearson' s correlation coefficient: R = 0. 90). Together these results suggest that examining changes within males may facilitate detection of paternal care adjustment and verifies that males facultatively reduce care in response to lowered paternity confidence, especially in species where high rates of cuckoldry are combined with high costs of caring to future reproductive success.
In this study, we address problems arising from the lack of empirical tests of theoretical predictions about the evolution of paternal care adjustment. In particular, measuring variation in paternity and the costs and benefits of paternal care within species is a major undertaking and it remains a challenge to think of ways how these factors can be experimentally manipulated to test existing theoretical predictions. By adopting a comparative approach, we have been able to exploit variation between species and our results suggest several important considerations for future studies of paternal care adjustment. Firstly, our study provides some guidance about the characteristics of species best suited to studies of paternal care adjustment. Specifically, the expectation of adjustment should be lowered in species with either low costs of care or low promiscuity. Secondly, we suggest that studies more closely address theoretical predictions by linking measures of adjustment with measures of costs of care (none of the measures in our adjustment dataset were directly linked with the measures of costs [Tables S1 and S2]). Thirdly, the interaction between promiscuity and cost reported here could be tested empirically within a single species by characterising the relationship between the strength of adjustment and the residual reproductive value of males. This could be achieved by exploiting individual variation in factors such as male age, timing of breeding or quality, which are expected to correlate with residual reproductive value. When we see males caring for the offspring of another male, it is possible to assume that they are doing so simply because of a failure to accurately determine paternity success. Although our analysis shows that males are not as constrained by lack of reliable cues to paternity as often thought, it remains the case that females seem to get away with promiscuous mating in some species, with cuckolded males continuing to provide care. Are cuckolded males that maintain care blissfully ignorant or selfless dupes? Our analyses suggest they are neither; instead, whether or not cuckolded males reduce paternal care is readily explained by the cost of paternal care and the risks of cuckoldry. More generally, cuckolded males provide a good example of how selection favouring tolerance can lead to the appearance of losing in an evolutionary arms race with cheats [16]. The finding that males show some degree of response to cuckoldry in the majority of species studied has implications for the evolution of paternal care more generally: we estimate that the extent to which females reduce paternal investment by engaging in promiscuous copulations is 12% on average within-species. By changing relatedness between nest mates, it has been shown that female promiscuity can drive transitions to and from cooperative breeding in birds [17]. By lowering relatedness between males and offspring, female promiscuity also has the potential to drive selection for reduced levels of paternal investment [18]–[20] and may ultimately cause the breakdown of biparental breeding systems [21], [22].
In most species where it has been studied, males do not abandon or reduce paternal care when they are cuckolded by other males. These observations have presented a long-standing challenge to our understanding of what drives selection for paternal care. Our analysis of cuckolded fathers from 50 species of birds, fish, mammals, and insects, however, shows that sometimes it pays for males to stick around. In the case of humans and burying beetles, this is because females are relatively monogamous—by deserting, it is most likely the case that fathers will be deserting their own young. In species such as the chacma baboon, males face a significant risk of cuckoldry, and face potentially high penalties in terms of future breeding success by wasting precious resources on the young of other males. Unlike in humans, promiscuous females in these species will almost certainly lose the support of her mate in the effort to raise her young to adulthood.
evolutionary ecology
animal behavior
biology
evolutionary biology
behavioral ecology
Why Do Cuckolded Males Provide Paternal Care?