Temperature variability is associated with the occurrence of extra-pair paternity in blue tits

In birds, extra-pair paternity (EPP) constitutes an alternative mating strategy, with potentially important fitness consequences for both males and females and their offspring. Several factors have been identified that can influence the occurrence of EPP, but the role of environmental variability has so far received relatively little attention. Using long-term data set from a wild population of blue tit (Cyanistes cearuleus) we assess the importance of ambient temperature in modulating the levels of extra-pair paternity. Here, we show that variability of local thermal conditions affects the occurrence of EPP. Specifically, we found that the probability of EPP increased with increasing variability in ambient temperature experienced by females prior to egg laying. This pattern is consistent with the idea of plastic female responses to unpredictable environmental conditions. Our results suggest that extra-pair mating may represent an adaptive behavioural strategy to compensate for possible negative effects of unpredictable environmental conditions. 

Methods
Study area
Our research spans the years 2008–2016 and is part of a long-term study conducted in a nest-box breeding population of the blue tits on the island of Gotland, Sweden (57°03′ N, 18°17′ E). In our population, females lay a single clutch per season and each year almost all breeding attempts are recorded and as many reproducing individuals as possible are captured, for a more detailed description of the study site and general field procedure (for details see Drobniak et al., 2022).

Genetic and paternity analyses
We took a blood sample (ca. 20µL) from nestlings on the second day after hatching and from adults when they were caught by mist-nets or inside the nest boxes while feeding 14-day-old nestlings, DNA was extracted from blood samples with Chelex following the procedure described in Griffiths et al. (1998). In the following EPP analyses, the number of microsatellite loci used to determine parentage varied between years. In 2009–2010 and 2012–2015, the paternity was identified using five microsatellite loci (Arct et al., 2013). In 2011, we used 15 microsatellite loci (Arct et al., 2022), for a more detailed description of parentage assignment in blue tits see also Arct et al (2017). In our population, each year on average 30% of nests contain at least one EPY (range 14 to 45%). In our population a relatively high proportion of females seek extra-pair paternity; however, we have a small proportion of extra-pair young in the nests – 7.09%. For this reason, we treated EPP as a binary response, as we did in other previous studies.

Temperature data
We acquired temperature data using the website of the Swedish Meteorological and Hydrological Institute (http://opendata-download-metobs.smhi.se/explore/?parameter=3). We obtained data from the meteorological station located in Hemse (56.92°N, 18.15°E; approximately 10 km north from the study area). Raw climate data were used to compute the following descriptive measures of the local variation in ambient temperature for a period of 14 days prior to the laying of the first egg for each clutch:

1.     mean ambient temperature (°C) calculated within those 14 days;

2.     temperature variability (i.e., variance of average daily temperatures across those 14 days, expressed in °C2).

References

Arct A, Drobniak SM, Podmokła E, Gustafson L, Cichoń M 2013 Benefits of extra-pair mating may depend on environmental conditions—an experimental study in the blue tit (Cyanistes caeruleus). Behav. Ecol. Sociobiol, 67, 1809-1815.
Arct A, Sudyka J, Podmokła E, Drobniak SM, Gustafsson L, Cichoń M. 2017 Heterozygosity–fitness correlations in blue tit nestlings (Cyanistis caeruleus) under contrasting rearing conditions. Evol. Ecol., 31, 803-814.
Arct A, Drobniak SM, Mellinger S, Martyka R, Gustafsson L, Cichoń M 2022 Extra‐pair paternity in Blue Tits (Cyanistes caeruleus) depends on the combination of social partners' age. Ibis, 164(2), 388-395.
Drobniak SM, Cichoń M, Janas K, Barczyk J, Gustafsson L, Zagalska‐Neubauer M 2022 Habitat shapes diversity of gut microbiomes in a wild population of blue tits Cyanistes caeruleus. J. Avian Biol., e02829. (https://doi.org/10.1111/jav.02829)]
Griffiths R, Double MC, Orr K, Dawson RJ 1998 A DNA test to sex most birds. Mol Ecol. 7(8):1071-5