Multiple hypotheses explain variation in extra‐pair paternity at different levels in a single bird family

Extra‐pair paternity (EPP), where offspring are sired by a male other than the social male, varies enormously both within and among species. Trying to explain this variation has proved difficult because the majority of the interspecific variation is phylogenetically based. Ideally, variation in EPP should be investigated in closely related species, but clades with sufficient variation are rare. We present a comprehensive multifactorial test to explain variation in EPP among individuals in 20 populations of nine species over 89 years from a single bird family (Maluridae). Females had higher EPP in the presence of more helpers, more neighbours or if paired incestuously. Furthermore, higher EPP occurred in years with many incestuous pairs, populations with many helpers and species with high male density or in which males provide less care. Altogether, these variables accounted for 48% of the total and 89% of the interspecific and interpopulation variation in EPP. These findings indicate why consistent patterns in EPP have been so challenging to detect and suggest that a single predictor is unlikely to account for the enormous variation in EPP across levels of analysis. Nevertheless, it also shows that existing hypotheses can explain the variation in EPP well and that the density of males in particular is a good predictor to explain variation in EPP among species when a large part of the confounding effect of phylogeny is excluded.     

High rates of extra‐pair paternity in two equatorial populations of rufous‐collared sparrow,Zonotrichia capensis

The latitudinal increase in extra‐pair paternity (EPP) rates in birds suggests broad selective benefits to low EPP rates in the tropics. However, we have few EPP data from tropical birds, particularly from species with close relatives at high latitudes. Here, we report EPP rates in two resident equatorial populations of rufous‐collared sparrow Zonotrichia capensis, a genus well‐represented at high latitudes. We found 64% and 60% of broods contained extra‐pair offspring, and 42% and 52% of all young were extra‐pair. EPP rates were similar in these populations, despite clear differences in elevation, temperature, rainfall, and breeding season length. These findings provide evidence that EPP rates in tropical birds can be as high as those observed in temperate birds, and suggest that the selective pressures acting on EPP rates vary markedly across tropical birds.     

Extra pair paternity in birds: a review of interspecific variation and adaptive function

The application of molecular genetic techniques has revolutionized our view of avian mating systems. Contrary to prior expectations, birds are only very rarely sexually monogamous, with 'extra-pair offspring' found in approximately 90% of species. Even among socially monogamous species, over 11% of offspring are, on average, the result of extra-pair paternity (EPP). Based on over 150 molecular genetic studies of EPP in birds, we review two topical areas: (i) ecological explanations for interspecific variation in the rate of EPP; and (ii) evidence bearing on the adaptive function of EPP. We highlight the remaining challenges of understanding the relative roles of genes and ecology in determining variation between taxa in the rate of extra paternity, and testing for differences between extra-pair offspring and those sired within-pair.     

Extra‐pair paternity in a population of Chilean Swallows breeding at 54 degrees south

Geographic patterns of variation in life‐history traits have puzzled researchers for decades. However, the widely accepted idea that mating systems exhibit a tropical–temperate latitudinal trend, with extra‐pair mating systems being the norm among temperate species and genetic monogamy the norm among tropical species, is supported by sparse data, particularly for birds breeding in the tropics and even more so for birds that breed in the southern hemisphere temperate zone. Our objective was to examine the genetic mating system of Chilean Swallows (Tachycineta meyeni) breeding at 54°S in Tierra del Fuego, Argentina. From 2006 to 2009, we examined the paternity of young in 52 broods. Contrary to predictions based on their congeners that breed at equivalent latitudes in the northern hemisphere, Chilean Swallows in our study had low rates of extra‐pair paternity (EPP), with 13.5% of nests (N = 52) having at least one extra‐pair young and 6.8% of all nestlings (N = 161) fathered by extra‐pair males. These rates are also lower than those reported for species of Tachycineta swallows that breed at tropical latitudes. We found no support for a tropical–south temperate latitudinal cline in EPP rates. The highly unpredictable weather of the island of Tierra del Fuego might be influencing parental investment at this site; small clutch sizes and low EPP rates are expected if biparental attention is crucial for chick survival and reproductive success for these aerial insectivores. We argue that the sparse sampling of mating systems in birds worldwide may have contributed to a misapprehension of a global pattern. More studies of tropical and south‐temperate systems are needed to build on theories based on a wider set of taxa.     

Territory configuration moderates the frequency of extra‐group mating in superb fairy‐wrens

The frequency of extra‐pair paternity (EPP) in socially monogamous birds varies substantially between and within species, but ecological drivers of this variation remain poorly understood. Habitat configuration could influence EPP by moderating access to extra‐pair mates, because species occupying territories in a clustered ‘honeycomb’ configuration have a larger pool of potential extra‐group mates in their immediate neighbourhood than those living in linearly arranged territories (e.g. along narrow strips of riparian or fragmented habitat). We exploited variation in the spatial arrangement of territories due to anthropogenic modification of habitat of the cooperatively breeding superb fairy‐wren Malurus cyaneus to test whether habitat configuration influenced the frequency of EPP. In this species, most paternity is obtained by males outside the social group [extra‐group paternity (EGP)]. We found that the frequency of EGP among groups living in linear strips of roadside vegetation (41% of 44 offspring) was lower than it was for groups living in clustered territories within continuous habitat (59% of 70 offspring). Differences in group size and pair relatedness did not explain differences in EGP associated with territory configuration, although the frequency of EGP was negatively correlated with pair relatedness. Our finding suggests that territory configuration can influence rates of EGP and that anthropogenic habitat fragmentation has the potential to limit access to extra‐pair mates, affecting mating systems and ultimately fitness.     

A continent‐scale test of multiple hypotheses on the abundances of Neotropical birds

Explaining variation in the abundance of species remains a challenge in ecology. We sought to explain variation in abundance of Neotropical forest birds using a dataset of population densities of 596 species. We tested a priori hypotheses for the roles of species traits, environmental factors, and species interactions. Specifically, we focused on four factors: 1) body mass (trait), 2) habitat type (environmental factor), 3) net primary productivity (NPP; environmental factor) and 4) species richness of competitors (species interaction). Body size explained much variation in density, although only when analyzed at higher taxonomic levels. Habitat type was a strong predictor of density. The relationship between density and productivity was weak. Densities were related negatively to the species richness of heterospecifics. This trend was particularly strong within closely related groups. Our results show that the influence of energetic factors such as body size and productivity depends on phylogeny, and that they act through indirect relations with other variables; alternative ecological factors such as habitat structure and species interactions play a more direct and stronger role in determining abundance than previously thought.     

High frequency of extra‐pair paternity in an urban population of Cooper's Hawks

Raptors exhibit some of the highest rates of intra‐pair copulations among birds, perhaps in an attempt by males to reduce the risk of being cuckolded. Indeed, the frequency of extra‐pair fertilizations reported in studies of raptors to date is relatively low (0–11.2%). Socially monogamous Cooper's Hawks (Accipiter cooperii) exhibit one of the highest copulation rates among birds, yet there are no published accounts of extra‐pair copulations (or paternity). We studied a population of Cooper's Hawks in Milwaukee, Wisconsin, during three breeding seasons (2003, 2004, and 2007), examining the possible effects of age (1 yr old vs. ≥ 2 yr old), adult mass, and brood size on the frequency of extra‐pair paternity (EPP). We found that 19.3% of nestlings (N = 27/140) were extra‐pair young (EPY), and 34% of all broods (N = 15/44) had at least one EPY. The sires of the EPY in our study were identified for only two broods, suggesting that floater males may have engaged in extra‐pair copulations with territorial females. We found that brood size was a good predictor of the occurrence of EPP (EPP) in nests, but adult mass and female age were not. To our knowledge, these possible correlates of the occurrence of EPP in raptors had not previously been investigated. Male Cooper's Hawks provide food for females during the pre‐nesting period, and delivery of food is, in contrast to other raptor species, typically followed by copulation. Thus, one possible explanation of the relatively high rates of EPP in our study is that females might accept or even solicit extra‐pair copulations from males other than their mates as a means of maximizing energy intake for egg production. Such behavior might be particularly likely in our study area, i.e., a food‐rich urban setting with a high breeding density of Cooper's Hawks.     

Differences in perceived predation risk associated with variation in relative size of extra‐pair and within‐pair offspring

Extra‐pair paternity (EPP) is a widespread phenomenon in birds. Researchers have long hypothesized that EPP must confer a fitness advantage to extra‐pair offspring (EPO), but empirical support for this hypothesis is definitively mixed. This could be because genetic benefits of EPP only exist in a subset of environmental contexts to which a population is exposed. From 2013 to 2015, we manipulated perceived predator density in a population of tree swallows (Tachycineta bicolor) breeding in New York to see whether fitness outcomes of extra‐pair and within‐pair offspring (WPO) varied with predation risk. In nests that had been exposed to predators, EPO were larger, longer‐winged and heavier than WPO. In nonpredator nests, WPO tended to be larger, longer‐winged and heavier than EPO, though the effect was nonsignificant. We found no differences in age, morphology or stress physiology between extra‐pair and within‐pair sires from the same nest, suggesting that additive genetic benefits cannot fully explain the differences in nestling size that we observed. The lack of an effect of predator exposure on survival or glucocorticoid stress physiology of EPO and WPO further suggests that observed size differences do not reflect more general variation in intrinsic genetic quality. Instead, we suggest that size differences may have arisen through differential investment into EPO and WPO by females, perhaps because EPO and WPO represent different reproductive strategies, with each type of nestling conferring a fitness advantage in specific ecological contexts.     

Global diversity and adaptations of avian eggshell thickness indices

The amniote eggshell is a fundamental aspect of the embryo life-support system, protecting it from UV light, microbes and mechanical damage, while regulating gas exchange and providing calcium for growth. The thickness of eggshells is highly diverse across modern birds and influences multiple eggshell functions, yet the selective pressures driving eggshell thickness have not been clearly identified. Here, we use a global dataset of avian eggshell thickness indices for 4260 (> 41%) avian species to assess trends in eggshell thickness across the phylogeny, as these indices are strongly correlated with direct measures of eggshell thickness and are non-destructive to the sample. We analysed the dataset within a phylogenetic framework to assess the relative importance of climatic and ecological explanations for variation in eggshell thickness indices. The distribution of avian eggshell thickness indices across species was found to be primarily driven by phylogenetic relatedness, in addition to evolutionary processes that do not match a Brownian model of evolution. Across modern birds, thicker eggshells were more prevalent in species (1) with precocial young, (2) which exhibit a scavenger-based diet, (3) which primarily feed on vertebrates or plants (excluding nectivores, seed and fruit specialists) and (4) which breed in open habitats. Thicker eggshells found in species with precocial young probably enable higher rates of calcium removal for the more advanced embryo development. Excessive light transmission through the shell damages developing embryos, while too little light transmission can impede development. Eggs in shaded habitats experience low light exposure, and thus thinner shells are more prevalent in these environments potentially to increase light transmission through the shell. Overall, variation in eggshell thickness indices appears to be driven largely by phylogeny, with certain life-history traits linked to embryo growth rate, calcium content of their food, and the need to mitigate excessive light transmission through the shell.     

Testosterone in tropical birds: effects of environmental and social factors

Previous investigations suggest that male tropical birds have lower plasma testosterone concentrations than northern latitude species. To test whether this generalization is valid, we analyzed all currently available plasma testosterone data of tropical birds. We focused on peak breeding testosterone levels using phylogenetic and conventional statistics. Explanatory variables considered were social mating system, type of territoriality, breeding season length, and altitude. On average, tropical birds had lower mean peak testosterone levels than northern temperate birds. However, in several tropical species, testosterone levels were well within the range of northern latitude birds. Without controlling for phylogeny, breeding season length, type of territoriality, and altitude explained a significant proportion of the variance in testosterone levels. The shorter the breeding season, the higher the testosterone levels. Tropical birds that defend a breeding season territory had higher testosterone levels than birds that were year-round territorial or colonial, and testosterone levels were positively correlated with altitude. When controlling for phylogeny, only breeding season length predicted testosterone levels. In conclusion, we propose to refine previous notions of low plasma testosterone levels in tropical birds: short breeding seasons and perhaps environmental conditions at high altitudes precipitate conditions under which high testosterone levels are beneficial in the tropics.     

New support for an old hypothesis: density affects extra‐pair paternity

Density has been suggested to affect variation in extra‐pair paternity (EPP) in avian mating systems, because increasing density promotes encounter rates and thus mating opportunities. However, the significance of density affecting EPP variation in intra‐ and interspecific comparisons has remained controversial, with more support from intraspecific comparisons. Neither experimental nor empirical studies have consistently provided support for the density hypothesis. Testing the density hypothesis is challenging because density measures may not necessarily reflect extra‐pair mating opportunities, mate guarding efforts may covary with density, populations studied may differ in migratory behavior and/or climatic conditions, and variation in density may be insufficient. Accounting for these potentially confounding factors, we tested whether EPP rates within and among subpopulations of the reed bunting (Emberiza schoeniclus) were related to density. Our analyses were based on data from 13 subpopulations studied over 4 years. Overall, 56.4% of totally 181 broods contained at least one extra‐pair young (EPY) and 37.1% of totally 669 young were of extra‐pair origin. Roughly 90% of the extra‐pair fathers were from the adjacent territory or from the territory after the next one. Within subpopulations, the proportion of EPY in broods was positively related to local breeding density. Similarly, among subpopulations, proportion of EPY was positively associated with population density. EPP was absent in subpopulations consisting of single breeding pairs, that is, without extra‐pair mating opportunities. Our study confirms that density is an important biological factor, which significantly influences the amount of EPP within and among subpopulations, but also suggests that other mechanisms influence EPP beyond the variation explained by density.     

Ecology has contrasting effects on genetic variation within species versus rates of molecular evolution across species in water beetles

Comparative analysis is a potentially powerful approach to study the effects of ecological traits on genetic variation and rate of evolution across species. However, the lack of suitable datasets means that comparative studies of correlates of genetic traits across an entire clade have been rare. Here, we use a large DNA-barcode dataset (5062 sequences) of water beetles to test the effects of species ecology and geographical distribution on genetic variation within species and rates of molecular evolution across species. We investigated species traits predicted to influence their genetic characteristics, such as surrogate measures of species population size, latitudinal distribution and habitat types, taking phylogeny into account. Genetic variation of cytochrome oxidase I in water beetles was positively correlated with occupancy (numbers of sites of species presence) and negatively with latitude, whereas substitution rates across species depended mainly on habitat types, and running water specialists had the highest rate. These results are consistent with theoretical predictions from nearly-neutral theories of evolution, and suggest that the comparative analysis using large databases can give insights into correlates of genetic variation and molecular evolution.     

A Contrast in Extra-Pair Paternity Levels on Mainland and Island Populations of Mediterranean Blue Tits

Extra‐pair copulation (EPC) is a widespread behaviour amongst birds, yet the rate of occurrence of extra‐pair offspring is highly variable both within and across species. Two populations of Mediterranean blue tits, Parus caeruleus, one on the mainland and the other on the island of Corsica, are characterized by high levels of extra‐pair paternity (EPP), with 14 and 25% of extra‐pair offspring (in 46 and 68% of the nests), respectively. The rate of EPP is significantly higher in the island population. Such high rates on Corsica contradict the predictions of higher mate fidelity and lower levels of EPP on islands. Despite expressing several traits that characterize an insular syndrome, blue tits of Corsica do not exhibit lower genetic variation which could be associated with low levels of EPP on islands. Furthermore, our results do not support any of the hypotheses that have been proposed so far to explain variation in EPP rates at the local level. We tentatively suggest that proximate Mediterranean constraints, especially consistent food shortage, prompt females to seek better breeding opportunities through a two‐step process including high rates of EPC and divorce.     

Deeply conserved susceptibility in a multi‐host,multi‐parasite system

Variation in susceptibility is ubiquitous in multi‐host, multi‐parasite assemblages, and can have profound implications for ecology and evolution in these systems. The extent to which susceptibility to parasites is phylogenetically conserved among hosts can be revealed by analysing diverse regional communities. We screened for haemosporidian parasites in 3983 birds representing 40 families and 523 species, spanning ~ 4500 m elevation in the tropical Andes. To quantify the influence of host phylogeny on infection status, we applied Bayesian phylogenetic multilevel models that included a suite of environmental, spatial, temporal, life history and ecological predictors. We found evidence of deeply conserved susceptibility across the avian tree; host phylogeny explained substantial variation in infection status, and results were robust to phylogenetic uncertainty. Our study suggests that susceptibility is governed, in part, by conserved, latent aspects of anti‐parasite defence. This demonstrates the importance of deep phylogeny for understanding present‐day ecological interactions.     

Extrapair paternity, migration, and breeding synchrony in birds

To understand interspecific patterns in the strength of sexualselection, variation in the costs and benefits of exercisingmate choice needs to be evaluated. One manifestation of sexualselection in birds is the occurrence of greatly variable levelsof extrapair paternity (EPP). A proposed general explanationfor this variation is that the benefits to females in seekingextrapair copulations vary in a predictable manner accordingto the degree of breeding synchrony because females are betterable to assess potential extrapair partners when males are simultaneouslyin breeding condition. This hypothesis predicts a latitudinaltrend in EPP because birds tend to breed more synchronouslyaway from the equator. Expanding on previous geographicallyand taxonomically restricted tropical/temperate comparisons,we used phylogenetically independent standardized linear contraststo show that this positive relationship persists when all birdspecies for which EPP estimates currently exist are considered.However, if a third factor covaries with latitude in the sameway as breeding synchrony and EPP, this relationship need notbe causal. Migration could also account for latitudinal variationin the benefits to females of pursuing EPP, if migration isassociated with (1) hasty or (2) inaccurate mate choice, (3)facilitated assessment of male quality through the condition-dependenceof arrival time, or (4) increased genetic variance in male quality.We show that migration distance is positively related to theproportion of EPP and that migration can statistically explainthe latitudinal trend in EPP, even when confounding factorsare simultaneously controlled. Hence, alternative explanationsfor latitudinal variation in EPP may be feasible, and carefulintraspecific tests are needed to assess their relative importanceand their implications for geographical variation in life-historyevolution.     

Body size explains interspecific variation in size–latitude relationships in geographically widespread beetle species

1. In most birds and mammals, larger individuals of the same species tend to be found at higher latitudes, but in insects, body size–latitude relationships are highly variable. 2. Recent studies have shown that larger‐bodied insect species are more likely to decrease in size when reared at increased temperature, compared with smaller‐sized species. These findings have led to the prediction that a positive relationship between body size and latitude should be more prevalent in larger‐bodied insect species. 3. This study measured the body size of > 4000 beetle specimens (12 species) collected throughout North America. Some beetle species increased in size with latitude, while others decreased. Importantly, mean species body size explained c. 30% of the interspecific variation in the size–latitude response. 4. As predicted, larger‐bodied beetle species were more likely to show a positive relationship between body size and latitude (Bergmann's rule), and smaller‐bodied species were more likely to show a negative body size–latitude relationship (inverse Bergmann's rule). 5. These body size–latitude patterns suggest that size‐specific responses to temperature may underlie global latitudinal distributions of body size in Coleoptera, as well as other insects.     

Comprehensive paternity assignment: genotype,spatial location and social status in song sparrows,Melospiza Melodia

Comprehensive, accurate paternity assignment is critical to answering numerous questions in evolutionary ecology. Yet, most studies of species with extra‐pair paternity (EPP) fail to assign sires to all offspring. Common limitations include incomplete and biased sampling of offspring and males, particularly with respect to male location and social status, potentially biasing estimated patterns of paternity. Studies that achieve comprehensive sampling and paternity assignment are therefore required. Accordingly, we genotyped virtually all males and >99% of 6‐day‐old offspring over 16 years in a song sparrow (Melospiza melodia) population and used three complementary statistical methodologies to attempt complete paternity assignment for all 2207 offspring. Assignments were highly consistent across maximum likelihood methods that used solely genotype data, and heuristic and integrated Bayesian analyses that included data describing individual locations. Sires were assigned to >99% of all genotyped offspring with ≥95% confidence, revealing an EPP rate of c. 28%. Extra‐pair sires primarily occupied territories neighbouring their extra‐pair offspring; spatial location was therefore highly informative for paternity assignment. EPP was biased towards paired territorial males, although unpaired territorial and floater males sired c. 13% of extra‐pair offspring. Failing to sample and include unpaired males as candidate sires would therefore substantially reduce assignment rates. These analyses demonstrate the integration of genetic and ecological information to achieve comprehensive paternity assignment and direct biological insight, illustrate the potential biases that common forms of incomplete sampling could have on estimated patterns of EPP, and provide an essential basis for understanding the evolutionary causes and consequences of EPP.     

Extra‐Pair Paternity Declines with Female Age and Wing Length in the Pied Flycatcher

Despite many studies of how male characteristics affect paternity in predominantly monogamous birds, relatively little attention has been given to the traits of females that may influence extra‐pair paternity (EPP). However, the occurrence of EPP may be the result of behavioural interactions in which both male and female traits are important for determining the outcome. If EPP is driven mainly by female choice of extra‐pair sires, older, more experienced or larger females would be better able to evade mate guarding tactics and more capable of selecting extra‐pair mates and resisting unwanted suitors. This would be especially noticeable in females paired with unattractive mates. On the other hand, if EPP is driven mainly by male pursuit, we should expect that young, inexperienced or small females would be more exposed to coercive male approaches independently of social mate traits. In a study of an Iberian population of the pied flycatcher Ficedula hypoleuca, we found that EPP affected 38% of the broods and 17% of the nestlings. These values are relatively high, allowing a relatively large number of affected within‐pair mates to be included. We found that EPP is related to both female and male traits although not to any interaction between male and female traits. EPP was higher at nests tended by both younger and short‐winged females and by browner males. Older females may be more experienced and dominant while long‐winged females may be faster fliers, these traits enabling them to avoid extra‐pair copulations, while brown males are less aggressive towards male intruders. In our study population, EPP appears to be caused by male pursuit, which in some cases may overwhelm female attempts to avoid extra‐pair copulations and their social partner's ability to prevent them.     

Mating strategies in dominant meerkats: evidence for extra‐pair paternity in relation to genetic relatedness between pair mates

Rates of extra‐pair paternity (EPP) have frequently been associated with genetic relatedness between social mates in socially monogamous birds. However, evidence is limited in mammals. Here, we investigate whether dominant females use divorce or extra‐pair paternity as a strategy to avoid the negative effects of inbreeding when paired with a related male in meerkats Suricata suricatta, a species where inbreeding depression is evident for several traits. We show that dominant breeding pairs seldom divorce, but that rates of EPP are associated with genetic similarity between mates. Although extra‐pair males are no more distantly related to the female than social males, they are more heterozygous. Nevertheless, extra‐pair pups are not more heterozygous than within‐pair pups. Whether females benefit from EPP in terms of increased fitness of the offspring, such as enhanced survival or growth, requires further investigations.     

Genetic monogamy in two long‐lived New Zealand passerines

High rates of extra‐pair paternity (EPP) can be relatively common in passerines whereas low rates or absence of EPP are often associated with taxa that are long‐lived and exhibit obligatory paternal care. We examined EPP in an under‐represented category: passerine species with relatively long life spans (or low annual mortality rates). Specifically, we studied EPP in New Zealand saddlebacks Philesturnus carunculatus and robins Petroica australis, two species with unusually low annual mortality rates (6.5–11% and 10–20% respectively). No EPP (0%) was detected in saddlebacks (39 pairs, 202 offspring) and only one case of EPP (1.9%) was detected in robins (54 pairs, 198 offspring). Genetic monogamy in these passerine species supports the hypothesis that low annual mortality rates play an important role in explaining variation in rates of EPP across species.