EPP and breeding density. Variation in breeding density is one of the traditional ecological explanations for interspecific variation in the rate of EPP. The relationship between breeding density and EPP has been examined in four ways: interspecific analysis across taxa; intraspecific comparisons between populations; intraspecific comparisons between different individuals within a single population; and meta-analysis of species-specific studies. We will review briefly each of these forms of evidence and demonstrate that, in general, there is little evidence of a general interspecific relationship between breeding density and the incidence of EPP in birds. Instead, the importance of breeding density appears limited to explaining differences between individuals in the same population, and possibly variation between different populations of the same species.
The hypothesis that interspecific variation in the rate of EPP is linked to breeding density appears to have arisen as an extrapolation from the observation that extra-pair copulations are more common among colonially nesting species than among species with more dispersed nests (e.g. Møller & Birkhead 1993). Such an extrapolation assumes, however, that the rate of EPP is closely correlated with the rate of extra-pair copulation, that colonially nesting species are typical of high nesting density species, and that raw species data can be used as independent data points. Subsequently, when these assumptions have been tested using molecular data on the rate of EPP per se and a more sophisticated interspecific comparative analyses, no robust evidence has been found for a relationship interspecific variation in the rate of EPP and breeding density (Westneat & Sherman 1997; Wink & Dyrcz 1999). There is therefore no strong evidence for the role of breeding density in determining interspecific variation in the rate of EPP.
The lack of a consistent relationship between breeding density and EPP in these intraspecific analyses does not necessarily reflect the total absence of an underlying biological relationship, but more probably the poor design of the tests. There are four common factors that undermine the strength of published studies of population differences in density and EPP: (i) the published studies have all been observational rather than experimental; (ii) the published studies have low statistical power due to the small number of populations involved (usually between two and four); (iii) there is usually very little variation between populations in both density and EPP; and (iv) the tests fail to acknowledge the large standard error around the estimates of EPP for any one population. So far, no published study of between-population variation in EPP and breeding density has controlled for all these problems.
An alternative intraspecific approach is to make comparisons between individuals in the same population, such as comparing the rate of EPP in pockets of the population breeding at high density with the rate in pockets breeding at low density. Using this approach, some workers have found a positive relationship between breeding density and EPP (e.g. Hill et al. 1994; Hoi & Hoi-Leitner 1997; Langefors et al. 1998; Richardson & Burke 1999), while others were unable to find a relationship between these variables (e.g. Barber et al. 1996; Sundberg & Dixon 1996; Verboven & Mateman 1997; Tarof et al. 1998; Chuang et al. 1999; Moore et al. 1999). Also, as part of their overall comparative study of the link between breeding density and the rate of EPP, Westneat & Sherman (1997) tested for an overall relationship between populations of the same species. While warning of a small sample size, they did report that there was a general trend for high density populations to have a higher rate of EPP than con-specific populations at lower density. This is arguably the strongest comparative evidence of a link between density and EPP, albeit at the level of differences among populations rather than differences among species. Of course, the weakness of any such comparative approaches is that the density at which individuals breed within a population will be dependent on other factors which may also covary with EPP. For example, low quality males may be forced to breed at higher density than more aggressive high quality males who defend a larger area around their nest. These studies are unable therefore to provide diagnostic evidence for a causal relationship between density and EPP, a familiar problem highlighting the need for experimental work.
To date only one study has investigated experimentally a possible relationship between density and EPP and unfortunately in this study paternity was determined using allozymes. In their study, conducted on nest box-breeding eastern bluebirds Sialia sialis, Gowaty & Bridges (1991) used nest box-placement to manipulate the densities of breeding pairs. This revealed a clear positive relationship between breeding density and EPP and remains the best experimental evidence of a link between density and EPP, albeit at the level of variation within a single population. Even in this case, however, it should be remembered that this experimental study consisted of a single comparison between a ‘high’ density population and ‘low’ density population and this test is equivalent to a sample size of one. More such studies are required to establish whether this is a general phenomenon.
A final approach to testing for the role of breeding density in determining the rate of extra-pair paternity is to perform a meta-analysis across single-species studies. Meta-analyses do not test for biological correlates of interspecific variation, but test whether there is evidence of a consistent relationship between two (or more) variables across a series of within-species studies (Rosenthal 1991). This meta-analysis approach was recently employed by Møller & Ninni (1998) to investigate a large range of factors that have been suggested to be associated with intraspecific variation in the rate of EPP. As part of this study Møller and Ninni found that, across studies, there was indeed consistent evidence of a relationship between breeding density and the rate of extra-pair paternity. This was true even when Møller and Ninni used a multivariate approach to control for the effect of variation in other factors, such as the extent of sexual dimorphism. This suggests strongly that breeding density is an important factor in determining variation in the rate of EPP between individuals or between families in the same study population.
In summary, there is little evidence that interspecific variation in the rate of EPP is due to variation in breeding density. If there is a relationship across species between breeding density and EPP then it is neither consistent nor strong, and variation in breeding density explains very little of the overall variation in EPP (see Westneat & Sherman 1997). This agrees with the prediction from phylogenetic analysis that much of the interspecific variation in the rate of EPP lies among ancient avian evolutionary lineages, which do not usually differ significantly from one another in terms of overall breeding density (Owens & Bennett 1997). There is good evidence, however, that breeding density may be important in determining variation in the rate of EPP at lower taxonomic levels. The most statistically robust evidence for this comes from Møller & Ninni (1998) meta-analysis, which shows that breeding density is associated consistently with variation in the rate of EPP among individuals in the same species. Westneat & Sherman's (1997) comparative studies also suggest that breeding density may play a role in determining variation in the rate of EPP between populations of the same species, although further experimental work along the lines of that pioneered by Gowaty & Bridges (1991) is required to establish whether this relationship is causal.
EPP and breeding synchrony. Variation in breeding synchrony is the other traditional ecological explanation for interspecific variation in the rate of EPP. Here, breeding synchrony refers to the proportion of females that are fertile at any one moment in time, so that high synchrony refers to a situation where many females are reproductively active at the same time. The potential importance of breeding synchrony as a determinate of interspecific variation in the level of EPP was first championed by Stutchbury & Morton (1995), who showed a positive correlation between these two variables in a comparison of 21 genera of passerines (later increased to 34 species; Stutchbury 1998a) (see also Birkhead & Biggins 1987). Based on this evidence Stutchbury and Morton suggested that in a synchronously breeding population, females are better able to compare between different males, facilitating their choice of extra-pair partners. Unfortunately, however, Stutchbury & Morton (1995) original analyses made no attempt to control for two factors that may potentially jeopardize the validity of the correlation: the phylogenetic relationships between species in the analysis; and the measurement error around the estimates of EPP. A subsequent comparative analyses that controlled for phylogeny and explored potentially confounding factors found no evidence of a relationship between EPP and breeding synchrony (Westneat & Sherman 1997), albeit with a much reduced sample size for breeding synchrony.
The difference in results between Stutchbury & Morton (1995) original analyses and Westneat & Sherman's (1997) subsequent analyses led to an exchange of published letters between Stutchbury (1998a,b) and Weatherhead & Yezerinac (1998). In these articles Stutchbury provides additional data of breeding synchrony and the rate of extra-pair paternity (Stutchbury 1998a), performs a comparative analyses based on using species as independent data points (Stutchbury 1998a), and then carries out two types of analyses to control for phylogenetic nonindependence: first a sister-taxa test on nine pairs of species (Stutchbury 1998a) then a test based on 33 phylogenetic independent contrasts (Stutchbury 1998b). All of these new tests show a significant correlation between breeding density and the rate of EPP, leading Stutchbury (1998a) to claim that ‘the breeding synchrony hypothesis remains the most viable explanation of the great variation in EPP frequency among bird species world-wide’. Although we regard this as being rather a strong claim considering the relatively small size of the database available at that time and the correlational nature of all comparative studies, we would agree with Stutchbury (1998b) that the breeding synchrony hypothesis has held up better in comparative tests than has the breeding density hypothesis.
Despite Stutchbury's (1998a,b) new phylogeny-based comparative analyses, Weatherhead & Yezerinac (1998) still had a major objection to the breeding synchrony hypothesis: namely that the correlational evidence of comparative studies is not supported by the available empirical tests. Weatherhead & Yezerinac (1998) argued that, if the level of synchrony generally does drive variation in levels of EPP between species, there should also be a relationship between populations within a species or between territories within a population. There is no such relationship in the Eastern blue bird Sialia sialis (Meek et al. 1994); tree swallow Tachycineta bicolor (Dunn et al. 1994); yellow warbler Dendroica petechia (Yezerinac & Weatherhead 1997); red-winged blackbird Agelaius caerulescens (Weatherhead 1997); blue tit Parus caeruleus (Kempenaers et al. 1997); American redstart Setophaga ruticilla (Perreault et al. 1998); house sparrow Passer domesticus (Griffith et al. 1999a); sedge warbler Acrocephalus schoenobaenus (Langefors et al. 1998); mangrove swallow Tachycineta albilinea (Moore et al. 1999); or serin Serinus serinus (Hoi-Leitner et al. 1999). Indeed, only two intraspecific studies have provided significant support for such a relationship, both within a single population. The most synchronous breeding families exhibited higher levels of EPP in both the clay-coloured robin Turdus grayi (Stutchbury et al. 1998), and the hooded warbler Wilsonia citrina (Stutchbury et al. 1997). This is, however, relatively weak evidence for a causal relationship between synchrony and rate of EPP due to the potential influence of uncontrolled confounding variables and the small number of independent comparisons. Also, negative relationships between synchrony and EPP have been demonstrated in the Eastern Phoebe Sayornis phoebe (Conrad et al. 1998), great tit Parus major (Strohbach et al. 1998), and barn swallow (Saino et al. 1999). The observational evidence on the empirical link between breeding synchrony and EPP is at best mixed, therefore.
To our knowledge only one published study has investigated experimentally (albeit inadvertently) the relationship between synchrony and EPP (Verboven & Mateman 1997). In a population of the great tit, the whole, or part, of the first clutch was removed provoking a second, more asynchronous breeding attempt. No difference was detectable in the levels of EPP in synchronous first broods and asynchronous second broods although levels of EPP were low throughout this whole population and the power of this test is very weak (Verboven & Mateman 1997). The only experimental evidence available does not, therefore, support the breeding synchrony hypothesis.
Overall, we suggest that, despite considerable empirical effort and much heated debate, it remains difficult to assess the role of variation in breeding synchrony in determining interspecific variation in EPP. Although Stutchbury (1998a,b) comparative analyses appear to provide phylogenetically robust correlational evidence for a link between these variables, it remains unclear whether this link is causal. We say this for three reasons. First, the key supportive comparative tests (Stutchbury 1998a,b) were performed on relatively small databases and the relative contribution of potentially confounding factors were not examined in detail. Second, we know that over 50% of the interspecific variation in EPP occurs among ancient avian lineages, rather than among closely related species, making it unlikely that a single ecological factor is going to explain all the variation among species. Finally, the empirical evidence for a causal link between breeding synchrony is not straightforward. Although many empirical studies have reported no association between the extent of breeding synchrony and the rate of EPP, Møller and Ninni's (1998) recent meta-analysis did identify breeding synchrony as a consistently important correlate. Given the lack of experimental studies of the influence of breeding synchrony, this contradiction is difficult to interpret biologically. We conclude that the breeding density hypothesis has not been falsified and could plausibly play a role in determining interspecific variation in EPP. To go further than this we need further comparative tests on the relative role of breeding density vs. other factors and experimental tests of whether there is indeed a causal link between breeding density and EPP. Without these forms of evidence we feel it is too early to say that the breeding synchrony hypothesis is either important or trivial.
EPP and genetic diversity. The difficulties in finding support for the traditional ecological hypotheses based on breeding density and breeding synchrony has led some authors to suggest that the key factor in determining interspecific variation in EPP may be genetic rather than demographic. Although genetic benefits have often been invoked to explain the reproductive behaviour of individual males and females (see Andersson 1994), Petrie & Lipsitch (1994) appear to have been the first to predict explicitly that interspecific variation in the rate of polygyny should be determined by the level of additive genetic variation. Using a game theory approach, Petrie & Lipsitch (1994) showed that, assuming that females suffered a cost from seeking to mate with more than one male, females should be more likely to mate with additional mates if there was extensive additive genetic diversity among those mates with respect to fitness. In terms of avian EPP, this theory has been taken to predict that EPP should be most common in those species with high genetic diversity (Petrie & Kempenaers 1998). This ‘genetic diversity hypothesis’ has been investigated both at the level of variation between different species and at the level of differences between populations of the same species.
As far as we are aware, the only published evidence of an interspecific correlation between genetic diversity and rate of EPP comes from two comparative studies combined by Petrie et al. (1998). In the first of these Petrie et al. (1998) collated data on the proportion of allozyme loci that were polymorphic across 35 species of bird and then used a phylogeny-based comparative approach to show that the level of EPP was positively correlated with the allozyme polymorphism. In a bivariate regression model based on evolutionarily independent contrasts, the proportion of polymorphic loci explained 22% of the variance in changes in the rate of EPP, but a multivariate model incorporating three other variables (level of sexual dichromatism, body size and sample size) explained 85% of the variation in EPP. In the second test the same authors identified seven phylogenetically matched-pairs of species or populations that differed significantly in terms of their rates of EPP, then obtained genetic samples for all of these populations and measured the proportion of polymorphism and gene diversity (approximated to average heterozygosity) at a series of random priming sites [random amplified polymorphic DNA (RAPD)]. In general the results supported the genetic diversity hypothesis, although the results were statistically significant only at the 10% level (in six of seven of the matched-pairs the taxon with the higher rate of EPP also had a higher rate of RAPD polymorphism (P = 0.06), while in five of the seven pairs the taxon with the higher EPP had a higher showed gene diversity (P = 0.08)). Nevertheless, when Petrie et al. (1998) used a combined probability test to maximize statistical power across both the allozyme and RAPD based tests, they found an overall effect of polymorphism significant at the 0.001% level. Although it must be kept in mind that these comparative tests are based on indices far removed from ‘additive genetic variation in male fitness’, it is none the less remarkable that such crude measures of genetic diversity can explain such a high proportion of variation in EPP among closely related taxa.
In addition to the matched-pairs test of Petrie et al. (1998), which includes a mixture of comparisons between species (five comparisons) and within species (two comparisons), the role of genetic diversity in determining variation in EPP among populations of the same species has been addressed by comparing mainland and island populations. Both Griffith et al. (1999a); Griffith (2000) and Møller (2000) have suggested that the rate of EPP is often unexpectedly low in island-dwelling populations. Thus, if it is assumed that island populations are genetically depauperate compared to their mainland counterparts, this observation is consistent with the genetic diversity hypothesis. Of course, for most of the species used in these island–mainland comparisons there is no quantitative evidence that the insular population are indeed genetically depauperate, but such an effect has been widely reported in birds as well as other organisms (Frankham 1997).
Our main conclusion from these comparative studies is that the genetic diversity hypothesis deserves more study. Although the interspecific studies are difficult to interpret because they are correlational and based on indirect indices of additive genetic variation in male fitness, they do show much stronger correlations than have ever been demonstrated for either breeding density and breeding synchrony. Ideally, the next stage of research would be to experimentally manipulate the extent of genetic diversity and then monitor both the short- and long-term effects on the level of EPP. We predict that the greatest potential of the genetic diversity hypothesis will be in explaining differences in the level of EPP among very closely related species and among populations of the same species.
EPP and the need for paternal care. Another response to the limited explanatory success of the two traditional ecological explanations for interspecific variation in EPP (breeding density and breeding synchrony) is the hypothesis that high rates of EPP should be associated with little need for paternal care. The idea that interspecific variation in the rate of EPP may be determined, in part at least, by the need for male care appears to have originated on at least three independent occasions: by Mulder et al. (1994), Birkhead & Møller (1996) and Gowaty (1996). The core prediction of these hypotheses is that females should be more likely to seek extra-pair copulations when they can rear offspring with little help from their male partner, and can therefore risk the cost of reduced parental care.
The general explanatory power of the hypothesis that rates of EPP are determined by the need for paternal care was first explored by Birkhead & Møller (1996), who used a species-based comparative approach to show that, as predicted, EPP rates tended to be comparatively low in species where male care was ‘essential’. Birkhead & Møller (1996) stressed, however, that their analysis was only preliminary and cautioned that further studies were required to improve scoring methods, and test for the effect of phylogenetic nonindependence (see Harvey & Pagel 1991). Accordingly, both Møller (2000) and Arnold & Owens (2002) performed a phylogeny-based comparative analysis to test whether high rates of EPP really are associated with little requirement for paternal care. As predicted, both studies found that interspecific variation in the rate of EPP was significantly negatively associated with variation in the direct effect of paternal care in terms of reproductive success (Fig. 3). Subsequently, the rate of EPP has also been shown to be significantly negatively associated to other indices of the role of paternal care, such as sex differences in the provision of various types of care and the total duration of different components of care (see Møller & Cuervo 2000; Bennett & Owens 2002). Importantly, all these associations remain qualitatively unchanged, whether the analyses are based on raw species values or evolutionarily independent contrasts (see Møller 2000; Arnold & Owens 2002; Bennett & Owens 2002), and in most cases they remain significant when multivariate tests are used to examine the importance of paternal care when controlling for other variables (Arnold & Owens 2002; Bennett & Owens 2002). Hence, interspecific variation in the extent of female constraint appears to vary across the same phylogenetic levels as does interspecific variation in the level of EPP (see Owens & Bennett 1997; Arnold & Owens 2002). There is therefore strong correlative evidence from several research groups for a link between interspecific variation in the need for paternal care and interspecific variation in the rate of EPP.
Figure 3. Association between interspecific variation in the rate of extra-pair paternity (EPP) and interspecific variation in male contribution to parental care. Extra-pair paternity is measured in terms of the total percentage of young that were fathered by males other than the social mates of the females (see Møller 2000 for details). Male contribution to care is measured as the reduction in reproductive success that females suffer when they care for a brood alone, as a percentage of the full reproductive success that females accrue when they care for a brood with the assistance of a male (see Møller 2000 for details). Statistics and solid line refer to log-linear regression using species as independent data points. Redrawn from raw data in the Appendix of Møller (2000).
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As far as we are aware, only a single empirical study has investigated experimentally the link between the need for paternal care and the incidence of EPP. In their study of EPP in the serin, Hoi-Leitner et al. (1999) manipulated the abundance of food around the nest during the fertile phase of the female. As predicted by the paternal care hypothesis, females breeding in areas of high food abundance (manipulated and unmanipulated) were found to have a higher incidence of extra-pair offspring in their broods (Hoi-Lietner et al. 1999). Thus, although this is only a single study, there is experimental support for a causal link between differences in parental care can lead to differences in the rate of EPP.
We conclude that there is relatively good evidence for a link between the need for paternal care and the rate of EPP. The correlational evidence is particularly strong, being based on phylogenetically robust tests on large data sets and controlling for several other factors, and is consistent with the observation that much of the interspecific variation in both EPP and the form of parental care occurs at high taxonomic levels. From this comparative evidence we suggest that ancient changes in the form of parental care may have influenced the large differences in EPP between major lineages of birds. It is more difficult to know the role that variation in parental care may play in explaining variation among more closely related species, or among populations of the same species, or even among individuals within the same population. More experimental studies of the type used by Hoi-Leitner et al. (1999) are required to test for a general causal link at these levels.
EPP and the rate of adult mortality. Another variable that has been suggested recently to explain interspecific variation in the rate of EPP is the rate of adult mortality. Again, the idea of a link between rates of mortality and EPP appears to have arisen independently at least twice: by Mauck et al. (1999) and Wink & Dyrcz (1999).
Based on a series of state-dynamic models, Mauck et al. (1999) predicted that ‘because males of species with short reproductive lifespans should tolerate higher EP[P] rates than should males of species with long reproductive lives, there should be greater range of EP[P] rates observed for species with short than long reproductive life spans’ (Mauck et al. 1999: 107). According to their model, for species with short reproductive lifespans abandonment of a reproductive event is never adaptive even in the face of extreme uncertainty of paternity because by that stage an alternative reproductive event is unlikely (Mauck et al. 1999). In consequence, high rates of EPP will only be evolutionarily stable in species with short reproductive lifespans. As they observed: ‘EP[P] rates observed in passerine birds range from 0%… to > 70%… , whereas in long-lived birds such as procellariiformes, EP[P] rates range from 0% to only 14%’ (Mauck et al. 1999: 107).
This prediction of an association between EPP and adult mortality history was tested using a species-based comparative method by Wink & Dyrcz (1999) and Arnold & Owens (2002), both of whom were able to confirm that variation in the rate of adult mortality explained nearly 50% of the variation in the rate of EPP (see Fig. 4). Indeed, it is very striking even from a visual inspection of the data in Fig. 4 that Mauck et al.′s (1999) verbal prediction is accurate. In species with annual mortality rates of less than 30% the rate of EPP very rarely rises above 20%, whereas in species with a higher rate of mortality the rate ranges from 0% to 95% (albeit in over two-thirds of these high mortality species the rate of EPP is above the 20% level). Also, the use of phylogeny-based comparative methods has shown that the association between EPP and adult mortality is intact even when analyses are based on evolutionarily independent contrasts (Arnold & Owens 2002; Bennett & Owens 2002). When evolutionarily independent contrasts are used to control for the effects of phylogeny, changes in the rate of adult mortality still account for approximately 25% of variation in changes in the rate of EPP (Arnold & Owens 2002), which agrees with the observation that both EPP rates and life history traits show extensive variation at the same ancient phylogenetic levels (Bennett & Owens 2002).
Figure 4. Association between interspecific variation in the rate of extra-pair paternity (EPP) and interspecific variation in the rate of adult mortality. Extra-pair paternity is measured in terms of the total percentage of young that were fathered by males other than the social mates of the females (see Wink & Dyrcz 1999 for details). Annual rate of adult mortality is based on studies of uniquely marked individuals (see Wink & Dyrcz 1999 for details). Statistics and solid line refer to log-linear regression using populations as independent data points. Redrawn from raw data in the Appendix of Wink & Dyrcz (1999).
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In the case of the mortality hypothesis, to our knowledge there have been no attempts to test experimentally for a causal relationship between the rate of mortality and the rate of EPP. Indeed, because the logic of this argument is based on changes over an evolutionary timespan, rather than facultative changes within an individual, such tests would not be straightforward. Other than by using long-term selection experiments, it may not be possible to perform elegant manipulations of life histories that last over tens of generations. We therefore conclude that, as with the parental care hypothesis, there is strong correlative evidence in support of of a link between adult mortality and EPP but a lack of experimental evidence for the causal nature of this relationship. Again, given that both adult mortality and the rate of EPP vary most extensively among ancient avian lineages, it seems most probable that changes in adult mortality played a role in the ancient diversification of sexual mating systems but that other factors may be more important in determining contemporary variation among populations and among individuals.