Linking behaviour to genetics
Whilst there is no consensus definition of behaviour in the literature (Levitis et al., 2009), behavioural traits do not differ fundamentally from any other class of traits, and many have been shown to have some degree of genetic underpinning (Bleakley et al., 2010; Fitzpatrick et al., 2005). Studying behaviour in extinct species is challenging (Hsieh and Plotnick, 2020), and understanding the relevance of behavioural studies to past evolutionary events can be difficult. Nevertheless, integrative studies combining genetics and behavioural ecology are essential to our understanding of the adaptive value (or lack thereof) of behaviours (Penke et al., 2007). This is of paramount importance to our understanding of evolution both past and present given that behaviour is the suite of traits by which ecological interactions (both inter and intraspecific) are directly mediated. Unfortunately, our understanding of chondrichthyan behaviour (Bres, 1993; Guttridge et al., 2009), let alone the genetic basis of behaviour is severely limited. This hampers our understanding of chondrichthyan evolution in much the same way as a lack of integration between morphology and genetics: without an understanding of the genetic architectures and adaptive landscapes underlying behavioural traits we are fundamentally constrained in our ability to understand behavioural evolution, how it has contributed to the evolution of phenotypic diversity observed in extant taxa, and how it may influence organismal evolution in the face of rapid environmental change. Of particular importance to contemporary populations, it is not possible to evaluate the posited ‘special’ role of behaviour in evolution without an understanding of the genetic basis of behavioural traits (Levis and Pfennig, 2016; McGlothin and Brodie III, 2009).
The importance of behaviour to evolution has long been understood (Corning, 2014), however recent integrative studies combining genetics and behavioural ecology point towards two phenomena of particular importance to our understanding of contemporary chondrichthyan evolution. Indirect genetic effects (IGEs) occur the genotype of one individual alter the phenotype of another (Wolf et al., 1998). These effects – which are often cryptic and difficult to detect – are important in an evolutionary context as they can modulate the response to selection (McGlothin and Brodie III, 2009), thus acting as ‘pacemakers’ of adaptive evolution (Bailey et al., 2018). The other phenomenon of particular importance is plasticity first evolution – the proposition that phenotypic plasticity (including behaviour, which is intrinsically plastic) may precede and facilitate adaptive evolution by providing the ‘raw material’ upon which selection can act in the absence of de novo, mutation-based adaptations (Levis and Pfennig, 2016; Perry et al., 2018). This, like IGEs, could increase the rate at which adaptive evolution occurs, although debate exists regarding the validity of such hypotheses (Levis and Pfennig, 2016). As many chondrichthyan populations have low effective population sizes (Pazmiño et al., 2017) and long generation times (Cailliet et al., 2005), both IGEs and plasticity first adaptations could play a major role in determining the vulnerability of contemporary populations to rapid environmental change, yet until know both of these phenomena have been ignored in the context of chondrichthyan evolution.
This lack of integration is driven by many of the same limitations affecting integration between genetics and morphology, and as such can be overcome using broadly similar methodological approaches (Figure 1). Studies of past selection may provide valuable insights into the evolution of behavioural traits (Eusebi et al., 2018; Grams et al., 2015), and quantitative genetic studies are valuable not only for uncovering the genetic basis of these traits (Bubac et al., 2020) but for providing direct evidence of IGEs and plasticity first evolution. The major difference is that whilst morphology is easily quantified, relatively little is known about chondrichthyan behavioural ecology (Bres, 1993; Guttridge et al., 2009), and most existing studies are descriptive or qualitative in nature. This will have to be overcome before quantitative genetic methodologies can be applied, and thus I suggest that future studies of chondrichthyan behaviour must focus on quantifying behavioural variation within and between populations.