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Effects of heterozygosity and MHC diversity on patterns of extra-pair paternity in the socially monogamous scarlet rosefinch

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Abstract

Extra-pair copulation without apparent direct benefits is an evolutionary puzzle that requires indirect fitness benefits to females to explain its ubiquity in socially monogamous mating systems. Using wild scarlet rosefinches (Carpodacus erythrinus), we tested if genetic benefits in the form of global (microsatellite) heterozygote advantage, adaptive genes (major histocompatibility complex), or complementary genes (using both markers) were responsible for female extra-pair mate choice, while considering that the benefits of mate choice may be conditional on female genotype. We found no evidence for assortative or relatedness-based mating (complementary genes), but higher MHC diversity, microsatellite heterozygosity, and condition were significantly related to male extra-pair paternity (EPP) success. In contrast, female probability of having extra-pair offspring decreased with increasing heterozygosity. Interestingly, extra-pair and within-pair males had higher heterozygosity than their female mates and extra-pair males had higher MHC supertype diversity. The only genetic difference between extra-pair and within-pair offspring was lower variance in MHC allelic diversity within extra-pair offspring, providing limited support for indirect genetic fitness benefits for the markers tested. Offspring had both higher neutral heterozygosity and number of MHC supertypes than adults, as well as significant identity disequilibrium, potentially suggesting that mates are chosen to increase offspring diversity in the period of the present study. Overall, our results point to an EPP heterozygote advantage for males, especially when involving less heterozygous females, and suggest that heterozygosity effects on reproduction may differ between the sexes.

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Acknowledgments

We thank J. Abbate, A. Courtiol, J. Rushmore, S. Baird, the Bryja and Albrecht lab groups, and two anonymous reviewers for helpful discussion and comments on previous manuscript versions. We thank the Institute of Vertebrate Biology and the “bird genetics” project funded by the Czech Science Foundation, Reg. No. P505/10/1871 for field and lab support. JCW was supported by the European Social Fund (ESF) and the state budget of Czech Republic through the Operational Program Education for Competitiveness (OPEC), Reg. No. CZ.1.07/2.3.00/30.0048.

Conflict of interest

All authors declare no conflict of interest.

Authorship

The project was designed by TA, JB, and PM; data was collected by TA, PM, MV, JS, and RP; pyrosequencing was designed by WB and JR, and genetic analyses were performed by MP and RP; JW, MP, and TA analyzed data for this paper, and JW, MP, JR, MV, JB, and TA wrote the manuscript.

Ethical standards

All protocols were noninvasive and adhered to the laws and guidelines of the Czech Republic (Czech Research Permit numbers 6628/2008-10001). All protocols were approved by the Animal Care and Use Committees at the Czech Academy of Sciences (041/2011) and Charles University (4789/2008-30).

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Authors and Affiliations

  1. Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, v.v.i., Květná 8, 603 65, Brno, Czech Republic

    J. C. Winternitz, M. Promerova, J. Bryja & T. Albrecht

  2. Institute of Botany, Academy of Sciences of the Czech Republic, v.v.i., Lidická 25/27, 657 20, Brno, Czech Republic

    J. C. Winternitz

  3. Department of Evolutionary Biology, Evolutionary Biology Center, Uppsala University, Norbyvägen 18D, 752 36, Uppsala, Sweden

    M. Promerova

  4. Department of Zoology, Faculty of Science, Charles University in Prague, Vinicna 7, 128 44, Prague 2, Czech Republic

    R. Polakova, M. Vinker, J. Schnitzer, P. Munclinger & T. Albrecht

  5. Institute of Environmental Sciences, Jagiellonian University, Gronostajowa 7, 30-387, Krakow, Poland

    W. Babik

  6. Evolutionary Biology Group, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614, Poznan, Poland

    J. Radwan

  7. Research Facility Studenec, Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Studenec 122, 675 02, Konesin, Czech Republic

    J. C. Winternitz

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  1. J. C. Winternitz
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  2. M. Promerova
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  3. R. Polakova
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  4. M. Vinker
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  5. J. Schnitzer
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  7. W. Babik
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  9. J. Bryja
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  10. T. Albrecht
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Correspondence to J. C. Winternitz.

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Communicated by D. Rubenstein

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Winternitz, J.C., Promerova, M., Polakova, R. et al. Effects of heterozygosity and MHC diversity on patterns of extra-pair paternity in the socially monogamous scarlet rosefinch. Behav Ecol Sociobiol 69, 459–469 (2015). https://doi.org/10.1007/s00265-014-1858-9

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