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.