Understanding Extra-Pair Mating Behaviour: A Case Study of Socially Monogamous European Pied Flycatcher (Ficedula hypoleuca) in Western Siberia

Abstract

Extra-pair copulation (EPC) occurred in most socially monogamous bird species. The mechanisms leading to the frequent occurrence of extra-pair offspring (EPO, EPY) in socially monogamous couples, as well as the ‘function’ of EPC, are the subjects of strong debates and raise many unanswered questions. We studied the relationship between extra-pair paternity (EPP) and the different characteristics of males and females in the European pied flycatcher in Western Siberia (Russia). The analysis was based on the genotyping of 232 males, 250 females, 1485 nestlings (250 nests). The European pied flycatchers were predominantly socially and genetically monogamous, but about 20% of birds could be involved in EPP. Loss of paternity tended to be more frequent in one-year-old males. EPCs could be multiple: one individual may have up to three extra-pair partners. The EPP rate was independent of the breeding time. The extra-pair mates of an individual were mainly its near neighbours. The EPC status of an individual was unrelated to most of its morpho-physiological traits. The occurrence of EPP was almost twice as high in females nesting in good quality territories. The fitness of within-pair offspring, EPO, paternal half-sibs of EPO and maternal half-sibs of EPO did not differ statistically significantly. Assuming very low heritability of extra-pair mating, we argued that EPCs could be incidental side effects (by-product) of selection. We believe that the evolution and maintenance of extra-pair mating are the episelective processes in the case of the European pied flycatcher.

Extra‐pair paternity is not repeatable between years in Pied Flycatchers (Ficedula hypoleuca): a role for social context

“…This suggests that the defensive capacity of males relative to their social competitors is more important than those of their partners to either attract foraying extra-pair males and avoid mate guarding or alternatively to escape from male intruders (Ramos et al 2014). Our study also contributes to recent investigations suggesting that no single factor can explain EPP patterns (Grinkov et al 2022), and that interactive effects of multivariate analyses per individual are needed (Brouwer & Griffith 2019). A hierarchical explanation for variation in the occurrence of extra-pair fertilizations was postulated by Griffith et al (2002), considering fundamental life history and socio-ecological parameters as well as individual characteristics.…”

The impact of small groups on pre‐ and postcopulatory sexual selection in polyandrous populations

“…In each population, individuals mated within small groups of three males and three females with one of five predefined mating distributions that differed in average polyandry (i.e., the mean number of male mating partners per female) ranging from 1.67 to 2.67 mates per female, and also differed in the standardized variance in male mating success (i.e., the opportunity for precopulatory sexual selection, $$$ {I}_M={\mathrm{VAR}}_M/{\overline{M}}^2 $$$; Appendix ). The range of average polyandry utilized here is biologically relevant given both behavioral and extra‐pair paternity studies indicate that the average number of mates per female often ranges between 1 and 2 males in primates (Qi et al, 2020; Reichard, 1995), in birds (Brekke et al, 2013; Dunn et al, 2009; Fiske & Kålås, 1995; Grinkov et al, 2022; Krietsch et al, 2022; Webster et al, 1995; Wetton et al, 1997), as well as in studies of polyandrous spiders and reptiles (Levine et al, 2015; Watson, 1998). Moreover, the range of polyandry per female of 1–3 mates in simulations represents the minimum and maximum possible levels of female polyandry when group sizes are constrained to within small groups of 3 males and 3 females, similar to experimental studies in systems such as flies, voles, and fowl (Collet et al, 2012; Mills et al, 2007; Morimoto et al, 2019).…”

Indirect genetic effects improve female extra-pair heritability estimates

“…To reflect the increased likelihood of older males siring extra-pair offspring, we included age as a fixed effect across all models (Girndt et al 2018). We did not include fine-scale environmental or social effects, which can potentially bias heritability estimates in closed systems (Germain et al 2016; Grinkov et al 2022).…”

“…Adaptive hypotheses seek to explain female participation in extra-pair behaviours in the context of indirect benefits - those that benefit her offspring. However, evidence for such benefits is sparce (Akçay and Roughgarden 2007; Arct, Drobniak, and Cichon 2015; Hsu et al 2015; Grinkov et al 2022). Indeed, studies even often suggest costs, both to extra-pair offspring (Schmoll et al 2009; Sardell et al 2012; Hsu et al 2014), and to promiscuous females (Forstmeier 2007; Matysioková and Remeš 2013; Schroeder et al 2016).…”