The ecological-evolutionary interplay: density-dependent sexual selection in a migratory songbird

Little is understood about how environmental heterogeneity influences the spatial dynamics of sexual selection. Within human-dominated systems, habitat modification creates environmental heterogeneity that could influence the adaptive value of individual phenotypes. Here, we used the gray catbird to examine if the ecological conditions experienced in the suburban matrix (SM) and embedded suburban parks (SP) influence reproductive strategies and the strength of sexual selection. Our results show that these habitats varied in a key ecological factor, breeding density. Moreover, this ecological factor was closely tied to reproductive strategies such that local breeding density predicted the probability that a nest would contain extra-pair offspring. Partitioning reproductive variance showed that while within-pair success was more important in both habitats, extra-pair success increased the opportunity for sexual selection by 39% at higher breeding densities. Body size was a strong predictor of relative reproductive success and was under directional selection in both habitats. Importantly, our results show that the strength of sexual selection did not differ among habitats at the landscape scale but rather that fine-scale variation in an ecological factor, breeding density, influenced sexual selection on male phenotypes. Here, we document density-dependent sexual selection in a migratory bird and hypothesize that coarse-scale environmental heterogeneity, in this case generated by anthropogenic habitat modification, changed the fine-scale ecological conditions that drove the spatial dynamics of sexual selection.     

Spatial distribution of nests constrains the strength of sexual selection in a warbler

In socially monogamous species, extra‐pair paternity may increase the strength of intersexual selection by allowing males with preferred phenotypes to monopolize matings. Several studies have found relationships between male signals and extra‐pair mating, but many others fail to explain variation in extra‐pair mating success. A greater appreciation for the role that ecological contingencies play in structuring behavioural processes may help to reconcile contradictory results. We studied extra‐pair mating in a spatial context in the common yellowthroat (Geothlypis trichas), a territorial wood warbler. Over the course of 6 years, we observed 158 breeding attempts by 99 males, resulting in a total of 369 nests and 520 sampled nestlings. The spatial distribution of territories varied greatly, with males having between 0 and 10 close neighbours and between three and 39 neighbouring nestlings close enough to represent extra‐pair siring opportunities. Both within‐pair and extra‐pair reproductive success increased with breeding density, but the opportunity for sexual selection and strength of selection varied with density. Total variance in reproductive success was highest at low density and was mostly explained by variation in within‐pair success. In contrast, at high density, both within‐pair and extra‐pair successes contributed substantially to variance in reproductive success. The relationships between plumage and extra‐pair mating also varied by density; plumage was under strong sexual selection via extra‐pair mating success at high density, but no selection was detected at low density. Thus, ecological factors that structure social interactions can drive patterns of sexual selection by facilitating or constraining the expression of mating preferences.     

Extra‐pair fertilizations contribute to selection on secondary male ornamentation in a socially monogamous passerine

Despite considerable research effort, it remains unclear whether extra‐pair fertilizations (EPF) drive the evolution of male secondary ornamentation in socially monogamous systems. In this study, we test the hypothesis that EPF contribute to the evolution or maintenance of male feather ornamentation in a sexually dichromatic passerine, the Scarlet Rosefinch, Carpodacus erythrinus. We show that the colouration of ornamental breast feathers is a good predictor of basic sources of variation in male annual reproductive output in rosefinches and that the annual realized reproductive success of males is positively associated with measures of ornamental colouration only when gains and losses because of EPF are considered. The results indicate that EPF in rosefinches may rely on absolute (good genes) rather than self referential (genetic complementarity) criteria of mate choice. Our study corroborates the potentially important role of EPF in the evolution and/or maintenance of elaborate male ornaments in socially monogamous taxa.     

Evidence of genetic monogamy in the lemur Indri (Indri indri)

Monogamy is a rare strategy among mammals but relatively common among primates. The study of the evolution of monogamy in mammals and primates is lacking empirical studies that assess the relationship between a pair‐living social organization and genetic monogamy. Sexual or genetic monogamy can only be assessed by performing molecular analyses and investigating rates of extra‐pair paternity (EPP). Studying the occurrence of EPP can provide valuable insights into reproductive strategies and their adaptive value. The indri is a pair‐living primate that lives in stable groups. Their social units are composed of the reproductive pair and up to four more individuals, but extra‐pair copulation (EPC) can occur. This raises the question of whether this event may or may not lead to EPP. Here, we investigated whether a pair‐living social organization corresponds to genetic monogamy in indris (Indri indri). We analyzed the paternity of 12 offspring from seven pairs using a set of six microsatellite loci on fecal samples (mean number of alleles 11.7 ± 1.8 (mean ± standard deviation). We found that in 92% of cases the genetic profile of the offspring matched the paired male of the group for all the loci considered. In the only case of paternity mismatch, the paternity assignment remained inconclusive. Our results show that I. indri genetic monogamy is the norm and supports the hypothesis that pair‐living social organization is associated with low EPP rate. Also, our results are in contrast with the hypothesis of infertility as a reason to engage in EPC for this species.     

Within‐population variation in social strategies characterize the social and mating system of an Australian lizard,Egernia whitii

The lizard genus Egernia has been suggested as an excellent model system for examining the evolution of sociality as it exhibits considerable diversity in social organization both between and within species. To date the majority of work examining the factors responsible for the evolution of sociality within Egernia has advocated a broad scale approach; identifying the social structure of specific species or populations and comparing the degree of sociality between them. However, we argue that significant advancements could also be gained by examining variation in social strategies within populations. Here we integrate a detailed, 3‐year, field‐based examination of social spacing and juvenile dispersal with molecular analyses of paternity to determine the social and mating system of a Tasmanian population of White's skink (Egernia whitii). We show that E. whitii live in small stable family groups consisting of an adult male, his female partner(s), as well as juvenile or sub‐adults individuals. In addition, while the mating system is characterized by considerable genetic monogamy, extra‐pair fertilizations are relatively common, with 34% of litters containing offspring sired by males from outside the social group. We also show that traits related to social organization (social group composition, group size, stability and the level of extra‐pair paternity) vary both between and within individuals. We suggest that ecological factors, such as habitat saturation, quality and availability, play a key role in maintaining between individual variation in social strategies, and that examining these individual level processes will allow us to more clearly understand variation in sociality among species.     

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.     

Sexual dimorphism and sexual selection in a montane scincid lizard (Eulamprus leuraensis)

Sex‐based divergences in body sizes and/or shapes within a species imply that selective forces act differently on morphological features in males versus females. That prediction can be tested with data on the relationship between morphology and reproductive output in females, and between morphology and realized paternity (based on genetic assignment tests) in males. In a sample of 81 field‐collected adult Blue Mountains water skinks (Eulamprus leuraensis), males and females averaged similar overall body sizes (snout–vent lengths (SVLs)). Reproductive success (based on 105 progeny produced by the females) increased with SVL at similar rates in both sexes (as expected from the lack of sexual size dimorphism). Multiple paternity was common. Males had larger heads than females of the same body size, and (as predicted) reproductive success increased with relative head size in males but not in females. Males also had relatively longer limbs and shorter trunks than females, but we did not detect significant sex differences in selection on those traits. Reproductive success in both sexes was increased by relatively longer hind limbs. Our data clarify mating systems in this endangered species, and suggest that mating systems are diverse within the genus Eulamprus.     

Field studies on a social lizard: Home range and social organization in an Australian skink,Egernia major

Abstract Although most reptiles have polygynous mating systems without long‐term pair bonds, one lineage of large scincid lizards in Australia is exceptional in this respect. Reports of complex sociality in the genus Egernia led us to conduct the first radiotelemetric field study of a species within this group. Land mullets (Egernia major) are large (60 cm total length), viviparous lizards from rainforest habitats in south‐eastern Australia. To document the spatial ecology and social organization of this species, we captured 12 adult lizards in the Barrington Tops area of eastern New South Wales and implanted them with miniature radiotransmitters. The lizards were released at their sites of capture and located daily for the next 6 weeks. All of the radiotracked lizards had discrete home ranges of approximately 10 000 m², based around well‐defined core areas (approximately 2000–3000 m²). Females tended to move further, and to range over wider areas, than did males. All of the radiotracked lizards lived in social groups consisting of one or more adult males and females plus juveniles of all age classes. Subgroups were apparent within one group of five radio‐tagged lizards: individual animals consistently shared their shelter sites and home ranges with one or more specific individuals. Male/female pairings were more frequent than expected under the null hypothesis of random association among individuals. The data in the present study support anecdotal reports of pair bonds in E. major and support suggestions that the social systems of species in this genus are more complex than those of previously studied reptiles.     

Genetic similarity, breeding distribution range and sexual selection

Large populations with extensive breeding distributions may sustain greater genetic variability, thus producing a positive relationship between genetic variation and population size. Levels of genetic variability may also be affected by sexual selection, which could either reduce levels because a small fraction of males contribute to the following generation, or augment them by generating genetic variability through elevated rates of mutations. We investigated to what extent genetic variability, as estimated from band sharing coefficients for minisatellite markers, could be predicted by breeding distribution range, population size and intensity of sexual selection (as reflected by degree of polygyny and extra-pair paternity). Across a sample of 62 species of birds in the Western Palearctic, we found extensive interspecific variation in band sharing coefficients. High band sharing coefficients (implying low local genetic variability among individuals) were associated with restricted breeding distributions, a conclusion confirmed by analysis of statistically independent linear contrasts. Independently, species with large population sizes had small band sharing coefficients. Furthermore, bird species with a high richness of subspecies for their breeding distribution range had higher band sharing coefficients. Finally, bird species with high levels of polygyny and extra-pair paternity had small band sharing coefficients. These results suggest that breeding distribution range, population size and intensity of sexual selection are important predictors of levels of genetic variability in extant populations.     

Inclusive fitness of 'kissing cousins': new evidence of a role for kin selection in the evolution of extra-pair mating in birds

Social monogamy is nearly ubiquitous across avian taxa,but evidence from a proliferation of studies utilizing molecular paternity analysis suggests that sexual monogamy is the rare exception rather than the rule (Griffith et al. 2002). Efforts to explain the prevalence of extra-pair paternity (EPP) have largely focused on the potential fitness benefits for offspring genetic quality, as females are less likely to benefit directly from seeking extra-pair mates. In particular, there has been considerable interest in the degree to which EPP may represent an adaptive female strategy to avoid inbreeding (or outbreeding)depression when paired with a highly related (or unrelated)social mate (Kempenaers 2007). Others have argued that, because relatives share many genes identical by descent,females might increase their own inclusive fitness by providing additional breeding opportunities to genetically related males (Waser et al. 1986; Kokko & Ots 2006). Thus, in the absence of significant inbreeding depression, pursuing EPP with relatives should be favoured by kin selection, although there exist few unambiguous empirical examples of such preferences in the literature. In this issue of Molecular Ecology, Wang &Lu (2011) present an analysis of mating patterns with respect to genetic relatedness of social and extra-pair partners in the ground tit (Parus humilis), a facultative cooperative breeder in which socially monogamous pairs occasionally form cooperative groups with unpaired helper males (Fig. 1). Consistent with the predictions of the kin-selection hypothesis, females in both bi-parental and cooperative groups preferentially engaged in extra-pair matings with relatives, irrespective of relatedness to their social mates, and while suffering no apparent costs of inbreeding depression in their progeny. These finding shave several exciting implications for our understanding of avian mating system diversity and the evolution of cooperative breeding.     

Female aggression predicts mode of paternity acquisition in a social lizard

Individual differences in behaviour are ubiquitous in nature. Despite the likely role of selection in maintaining these differences, there are few demonstrations of their fitness consequences in wild populations and, consequently, the mechanisms that link behavioural variation to variation in fitness are poorly understood. Specifically, the consequences of consistent individual differences in behaviour for the evolution of social and mating strategies have rarely been considered. We examined the functional links between variation in female aggression and her social and mating strategies in a wild population of the social lizard Egernia whitii. We show that female Egernia exhibit temporally consistent aggressive phenotypes, which are unrelated to body size, territory size or social density. A female''s aggressive phenotype, however, has strong links to her mode of paternity acquisition (within- versus extra-pair paternity), with more aggressive females having more offspring sired by extra-pair males than less aggressive females. We discuss the potential mechanisms by which female aggression could underpin mating strategies, such as the pursuit/acceptance of extra-pair copulations. We propose that a deeper understanding of the evolution and maintenance of social and mating systems may result from an explicit focus on individual-level female behavioural phenotypes and their relationship with key reproductive strategies.     

Social organization in Eulipotyphla: evidence for a social shrew

Shrews and their close relatives (order Eulipotyphla) are typically considered to be solitary. This impacts our understanding of mammalian social evolution: (i) the ancestor of mammals is believed to have been shrew-like, and even though Eulipotyphla are not more basal than other mammalian orders, this might have been one reason why the first mammals have been assumed to be solitary-living; (ii) Eulipotyphla are the third largest mammalian order, with hundreds of species entering comparative analyses. We review primary field studies reporting the social organization of Eulipotyphla, doing a literature research on 445 species. Primary literature was only available for 16 of the 445 species. We found 56% of the studied species to be social (38% were living in pairs), which is in sharp contrast to the 0.5 and 8% reported in other databases. We conclude that the available information indicates that shrews are more sociable than generally believed. An interesting alternative hypothesis is that the mammalian ancestor might have been pair-living. To understand the social evolution of mammals, comparative studies must be based on reliable and specific information, and more species of all orders must be studied in the field.     

Isolation and characterization of microsatellites in European alpine marmots (Marmota marmota)

For future investigations of the mating system of a highly social mammal (Marmota marmota), we identified 16 new microsatellites using an enrichment protocol. Five loci were revealed to be polymorphic. The polymorphism was rather low (two to six alleles among 24 individuals). However, these markers, added to the other six published microsatellites for M. marmota and Spermophilus citellus, will help to assess dispersal patterns and test for genetic monogamy in alpine marmots from the European Alps.     

Development of microsatellite markers for parentage analysis in the great tinamou (Tinamus major)

Eighteen microsatellite loci were isolated from great tinamous (Tinamus major), which are large terrestrial birds found in the Neotropics. These are the first primers developed for the Order Tinamiformes. Paternity analyses are possible because the levels of heterozygosity are sufficiently high (0.29-0.90).     

Age‐dependent changes in infidelity in Seychelles warblers

Extra‐pair paternity (EPP) is often linked to male age in socially monogamous vertebrates; that is, older males are more likely to gain EPP and less likely to be cuckolded. However, whether this occurs because males improve at gaining paternity as they grow older, or because “higher quality” males that live longer are preferred by females, has rarely been tested, despite being central to our understanding of the evolutionary drivers of female infidelity. Moreover, how extra‐pair reproduction changes with age within females has received even less attention. Using 18 years of longitudinal data from an individually marked population of Seychelles warblers (Acrocephalus sechellensis), we found considerable within‐individual changes in extra‐pair reproduction in both sexes: an early‐life increase and a late‐life decline. Furthermore, males were cuckolded less as they aged. Our results indicate that in this species age‐related patterns of extra‐pair reproduction are determined by within‐individual changes with age, rather than differences among individuals in longevity. These results challenge the hypothesis—based on longevity reflecting intrinsic quality—that the association between male age and EPP is due to females seeking high‐quality paternal genes for offspring. Importantly, EPP accounted for up to half of male reproductive success, emphasizing the male fitness benefits of this reproductive strategy. Finally, the occurrence of post‐peak declines in extra‐pair reproduction provides explicit evidence of senescence in infidelity in both males and females.     

Promiscuity drives sexual selection in a socially monogamous bird

Many socially monogamous species paradoxically show signs of strong sexual selection, suggesting cryptic sources of sexual competition among males. Darwin argued that sexual selection could operate in monogamous systems if breeding sex ratios are biased or if some males attract highly fecund females. Alternatively, sexual selection might result from promiscuous copulations outside the pair bond, although several recent studies have cast doubt on this possibility, in particular by showing that variance in apparent male reproductive success (number of social young) differs little from variance in actual male reproductive success (number of young sired). Our results from a long-term study of the socially monogamous splendid fairy-wren (Malurus splendens) demonstrate that such comparisons are misleading and do not adequately assess the effects of extra-pair paternity (EPP). By partitioning the opportunity for selection and calculating Bateman gradients, we show that EPP has a strong effect on male annual and lifetime fitness, whereas other proposed mechanisms of sexual selection do not. Thus, EPP drives sexual selection in this, and possibly other, socially monogamous species.     

Mating system, sexual dimorphism, and the opportunity for sexual selection in a territorial ungulate

In mammals, species with high sexual size dimorphism tend tohave highly polygynous mating systems associated with high variancein male lifetime reproductive success (LRS), leading to a highopportunity for sexual selection. However, little informationis available for species with weak sexual size dimorphism. Ina long-term study population, we used parentage analysis basedon 21 microsatellite markers to describe, for the first time,variance in male lifetime breeding success (LBS) of roe deer,a territorial ungulate where males weigh less than 10% morethan females. LBS ranged from 0 to 14 (mean = 4.54, variance= 15.5), and its distribution was highly skewed, with only afew males obtaining high LBS and many males failing to breedor siring only one fawn. As predicted for polygynous specieswith low sexual size dimorphism, the standardized variance inmale LBS was low (I_m = 0.75) and was only slightly higher thanthe standardized variance in female LRS (I_f = 0.53), suggestinga low opportunity for sexual selection. The I_m value reportedhere for roe deer is much lower than values reported for highlydimorphic ungulates such as red deer (I_m > 3). We suggestthat, along a continuum of opportunity for sexual selection,roe deer occupy a position closer to monogamous and monomorphicterritorial ungulates than to highly polygynous, sexually dimorphicungulates with dominance rank–based mating systems suchas harems or roving mating systems.