Factors influencing the expression of behaviour: maternal effects

The expression of behaviour, in general, in mammals can be influenced by multiple factors. I’ll start by explaining how maternal effects may influence an offspring’s behaviour.

Maternal effects have been defined by Wolf & Wade (2009) as “the causal influence of the maternal genotype or phenotype on the offspring phenotype.” While the mother’s genotype can influence the phenotype of the offspring, maternal effects are mediated through the mother’s phenotype (Wolf & Wade 2009). Maternal effects can influence the young while they are still in utero or during the early postnatal period (Liu et al. 1997). These maternal effects, primarily hormonally driven, have either a direct or an indirect organising effect on an offspring’s behavioural phenotype, hence these can be termed “organisational effects”. These organisational hormonal effects can create permanent, non-reversible changes in neural substrates underlying behaviour (Elekonich & Robinson, 2000).

Females may directly influence the offspring through cross placental hormonal transmission during gestation (Soares et al. 2010). Reproductive hormones, such as oestrogen (Goebelsmann etal. 1972) and stress hormones, such as cortisol (Van den Bergh et al. 2005) can be passed across the placenta during gestation. Furthermore, there is strong evidence that these hormones influence a variety of different behaviours (e.g. spatial memory and ability, Williams et al. 1990; Williams & Meck 1991; social behaviour, Mogi et al. 2014). For example, early exposure to oxytocin improves alloparental responsiveness in ICR mice (Fig. 1).

Fig. 1. Domestic mouse Mus musculus domesticus, ICR strain 

(Unknown: picture accessed 08 December 2014; 17h39) 

(http://www.taconic.com/icr)

Females can also influence an offspring’s phenotype indirectly through provision of postnatal care. Numerous studies have shown that variations in the quality and quantity of maternal care can influence their offspring’s behaviour later in life (e.g. Champagne et al. 2001; Jia et al. 2011). A classic example is seen in rats (Francis et al. 1999). Females that receive high levels of postnatal care during early development become mothers that also show high levels of care to their own offspring (Francis et al. 1999). Importantly, both sons and daughters are influenced by maternal effects. In African striped mice Rhabdomys pumilio (Fig. 2), sons experiencing high levels of care from their mothers show correspondingly high levels of paternal care to their own offspring later (Rymer & Pillay 2011).

Fig. 2 African striped mouse family Rhabdomys pumilio  

(Tasmin Rymer: personal picture)

 

In my next post, I explain how activational effects influence the expression of behaviour.

The development of paternal care

Although increasing in popularity, relatively few studies have investigated the how paternal care behaviour develops and is expressed, and what role fathers play in these processes.Bester-Meredith &Marler (2003) showed that a decrease in paternal care behaviour by California mouse Peromyscus californicus results in sons also showing lower levels of care, possibly because vasopressin expression in the bed nucleus of the stria terminalis (BNST) facilitates this behaviour. However, Bredy et al. (2004) found no apparent influence of paternal care on the development of the hippocampus, the area of the brain that secretes vasopressin.

Behaviour, in general, is influenced genetically and non-genetically (e.g. learning, Cushing & Kramer 2005), although behavioural expression can be more strongly influenced either by environmental or genetic components. For example, offspring feeding rate in long-tailed tits Aegithalos caudatus (Fig. 1) has a significant heritable component (MacColl & Hatchwell 2003), whereas paternal state is strongly regulated by environmental cues in meadow voles Microtus pennsylvanicus (Fig. 2), a species that is rarely paternal (Parker& Lee 2001). However, few studies have looked at the relative influence of both genetic and non-genetic factors on the development of paternal care.

 

Fig. 1 Long-tailed tit Aegithalos caudatus
(Tim Edelsten: picture accessed 28 July 2014; 12h53)
(http://www.birdskorea.org/Birds/Birdnews/BK-BN-Review-2007.shtml)

Fig. 2 Juvenile meadow vole Microtus pennsylvanicus
(Unknown: picture accessed 28 July 2014; 12h59)
(http://natchem.wordpress.com/2010/06/04/the-genetics-of-monogamy-guys-girls-you-better-read-this/)




In two recent studies, Prof. Neville Pillay (University of the Witwatersrand) and I demonstrated the importance of both non-genetic (Rymer & Pillay 2011a) and genetic (Rymer & Pillay 2011b) factors on the developmental of paternal care behaviour in biparental African striped mice Rhabdomys pumilio (Fig. 3). We found that mothers are particularly important for the development of paternal care behaviour in their sons (Rymer & Pillay 2011a). Sons raised by their mothers only show heightened levels of paternal care as adults, as mothers compensate for the absence of the father by increasing the amount of maternal care invested in their sons (Rymer & Pillay 2011a). Interestingly, there appears to be little genetic heritability of paternal care either down the matriline or the patriline (Rymer & Pillay 2011b), suggesting that the development of paternal care in striped mice in strongly regulated by environmental factors.

Fig. 3 Juvenile striped mice Rhabdomys pumilio

(Gaby Schmohl: picture accessed 28 July 2014; 16h10)
(http://www.stripedmouse.com/site1_3.htm)


In my next blog, I’ll make a start on those factors influencing the expression of paternal care.