Variation in parent-offspring kinship in socially monogamous systems with extra-pair reproduction and inbreeding.

Jane M Reid,Pirmin Nietlisbach,Matthew E Wolak,Elizabeth A Gow,A Bradley Duthie,Peter Arcese,Greta Bocedi

doi:10.1111/evo.12953

Abstract

Female extra‐pair reproduction in socially monogamous systems is predicted to cause cuckolded socially‐paired males to conditionally reduce paternal care, causing selection against extra‐pair reproduction and underlying polyandry. However, existing models and empirical studies have not explicitly considered that cuckolded males might be related to their socially‐paired female and/or to her extra‐pair mate, and therefore be related to extra‐pair offspring that they did not sire but could rear. Selection against paternal care, and hence against extra‐pair reproduction, might then be weakened. We derive metrics that quantify allele‐sharing between within‐pair and extra‐pair offspring and their mother and her socially‐paired male in terms of coefficients of kinship and inbreeding. We use song sparrow (Melospiza melodia) paternity and pedigree data to quantify these metrics, and thereby quantify the joint effects of extra‐pair reproduction and inbreeding on a brood's total allelic value to its socially‐paired parents. Cuckolded male song sparrows were almost always detectably related to extra‐pair offspring they reared. Consequently, although brood allelic value decreased substantially following female extra‐pair reproduction, this decrease was reduced by within‐pair and extra‐pair reproduction among relatives. Such complex variation in kinship within nuclear families should be incorporated into models considering coevolutionary dynamics of extra‐pair reproduction, parental care, and inbreeding.

Highlights

Identifying components of negative and positive selection that shape the evolution and persistence of extra-pair reproduction in socially monogamous systems remains a central challenge in evolutionary ecology (Arnqvist and Kirkpatrick 2005; Parker and Birkhead 2013; Reid et al 2015a)
In systems with biparental care, it is widely predicted that cuckolded socially-paired males, who have lost the paternity of extra-pair offspring (EPO) produced by their socially-paired female, should under some circumstances reduce their provision of costly paternal care rather than invest in broods that contain unrelated EPO that they did not sire (Sheldon 2002; Kokko and Jennions 2008; Alonzo 2010; Alonzo and Klug 2012; Griffin et al 2013)
within-pair offspring (WPO) DATA The 1526 observed WPO occurred in 639 broods produced by 196 females and 200 socially-paired males, spanning 318 different social pairings

Summary

Introduction

Identifying components of negative and positive selection that shape the evolution and persistence of extra-pair reproduction in socially monogamous systems remains a central challenge in evolutionary ecology (Arnqvist and Kirkpatrick 2005; Parker and Birkhead 2013; Reid et al 2015a). It is not widely noted that it is somewhat contradictory to hypothesize that any selection against female extrapair reproduction that arises because females’ cuckolded sociallypaired males reduce paternal care for unrelated EPO could be balanced by positive selection stemming from reduced inbreeding depression in females’ EPO. This is because, for extra-pair reproduction to reduce the degree to which a female’s offspring are inbred, the female must be related to her socially-paired male. Socially-paired males could be closely related to EPO that they did not sire but could rear

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Results

Conclusion