Genetic and Social Transmission of Parental Sex Roles in Zebra Finch Families

Boglárka Morvai,Ádám Miklósi,Emese Alexandra Fazekas,Ákos Pogány

doi:10.3389/fevo.2021.799996

Abstract

Parental care plays a central, reinforcing role in the evolution of sex roles and its development is often reported to be driven by genetic, rather than environmental effects. Based on these studies, however, genetic inheritance does not account fully for the often-significant phenotypic variability observed within species, a variation that we hypothesized may be explained by social effects from parents. Following a full cross-fostering design, here we aimed at disentangling genetic and social parental effects in the ontogeny of parental behaviours. Clutches of eggs were swapped, and we monitored parental behaviours in two consecutive generations of a captive population of the socially monogamous, biparental zebra finch (Taeniopygia guttata). Using nest box cameras, parental behaviour was recorded for 3 h in two reproductive stages: on day 8 of incubation and day 10 post-hatching. These fostered birds, after becoming fully matured, received a pair randomly and we observed parental care of this second generation too, following the same protocol. We then compared various parental behaviours (such as time spent incubating, or number of nest attendances during offspring provisioning) in the second generation to those of their genetic and social parents. Based on the results of our experiment, both genetic and social effects can contribute to intergenerational transmission of specific parental behaviours, with various weights. However, the strongest and most consistent effect that we found is that of the current mate; a social effect that can manifest both in negative and positive directions, depending on the behavioural trait. Our study suggests context-specific and sexually different genetic, social and non-social environmental effects in the ontogeny of parental sex roles and outline the importance of parental negotiation in explaining individual variation of parental behaviour in biparental species.

Highlights

Males and females often differ in various aspects of their reproductive behaviours, for instance, in their competitiveness and choosiness during mating and their parental behaviour, so that they exhibit distinctive sex roles (Kokko et al, 2006; Fairbairn, 2013)
Parental sex role differences in terms of workload may manifest in one parent providing full care and the other providing no care at all, or it may manifest in unequal relative amount of care provided by the two sexes in biparental systems
Male and female nest attendance frequencies were not explained by the genetic or social parents’ behaviour, we found positive correlation between the behaviour of pair members [LMM of hourly male nest attendance rate, effect of pair’s attendance rate: likelihood ratio tests (LRT): χ21 = 6.48, p = 0.011; exp(β) = 1.13 [1.03; 1.25], t15 = 2.59, p = 0.021; Figure 2A]

Summary

Introduction

Males and females often differ in various aspects of their reproductive behaviours, for instance, in their competitiveness and choosiness during mating and their parental behaviour, so that they exhibit distinctive sex roles (Kokko et al, 2006; Fairbairn, 2013). Sex-roles involve social behaviours, and as such, understanding how they change, develop, and evolve in non-human animals by genetic evolution, social learning and the interaction between them is challenging. Large adaptive value, and the prevalence of social learning are expected in situations when genetically determined behavioural variability is unproductive, non-social learning is costly or individuals are faced with uncertain, frequently changing environment (Laland, 2004; Rendell et al, 2011; Heyes and Pearce, 2015; Kendal et al, 2018); see Rieucau and Giraldeau (2011) for a detailed review on the costs and benefits of social learning). Vertical (from parents to offspring) or oblique transmission (from non-parent adults to offspring) is expected if environmental changes are not significant between subsequent generations, and horizontal transmission (between peers, either immatures or adults) is expected when environment changes rapidly, e.g., from generation to generation (Cavalli-Sforza and Feldman, 1981; Laland and Kendal, 2003)

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