Linking morphology to genetics
Comparative morphological studies of vertebrate anatomy and
morphogenesis have contributed significantly to our understanding of
evolutionary history and taxonomic interrelationships (Lee and Palci,
2015), and this is no different in Chondrichthyes (Naylor et al., 2005;
Shirai, 1996). Despite this, the interrelationships of various
chondrichthyan subclades have long been debated (Klug, 2010; Naylor et
al., 2005; Qiao et al., 2016), and it is only relatively recently, upon
the development of molecular phylogenies with high taxonomic coverage
(Naylor et al., 2005; Stein et al., 2018) that these controversies have
been resolved. Phylogenetics is likely the most universally applicable
integration of genetics and morphology, however increasingly
evolutionary-developmental (evo-devo) studies and evolutionary genetics
are being used to uncover the genetic basis of morphological traits
(Abzhanov et al., 2002; Mallarino and Abzhanov, 2012) and the selective
regimes under which they have evolved (Ho et al., 2017; Rolland et al.,
2018). Evo-devo studies targeting chondrichthyan taxa are present in the
literature, yet these target the expression of a small number of
morphological characters in a minute proportion of extant species
(Gillis et al., 2009; Gillis et al., 2013). Besides this, we have
extremely minimal knowledge of the genetic and developmental
underpinnings of morphological variation in Chondrichthyes.
This of course represents a knowledge gap in itself, but also
fundamentally constrains our ability to understand morphological
evolution within Chondrichthyes. Most such studies rely on an
ecomorphological approach (Gayford et al., 2023) under the assumption
that ecological selection is dominant and has shaped the evolution of
morphological structures (Andrew-Barr, 2018). Crucially, these studies
typically negate the potential role of constraint in morphological
evolution (Gayford et al., 2023). The importance of these constraints to
morphological evolution in other taxa is well known (Beldade et al.,
2002; Wagner, 1996), however such an understanding relies upon knowledge
of the genetic architectures or gene regulatory networks underlying
morphology (Davidson and Erwin, 2006; Hegmann and Possidente, 1981).
Evolutionary constraints such as genetic correlations can substantially
alter the pace of evolution by modulating the response to selection
(Crespi, 2000; Greenbury et al., 2016), whilst others such as lack of
additive variance can make ‘optimal’ genotypes effectively unattainable
(Hansen et al., 2003) or result in maladaptive evolution (Crespi, 2000).
There is debate surrounding the extent to which short-term genetic
constraints influence long-term evolution (Dooren, 2020; Hadfield et
al., 2007), however even if we ignore mounting evidence regarding the
importance of such constraint to past evolution (Futuyma, 2010), the
relevance of these concepts to the immediate future of chondrichthyans
and their contemporary evolution is unquestionable: in light of their
dire conservation status (Dulvy et al., 2021; Stein et al., 2018), low
fecundity, and long generation times (Cailliet et al., 2005), an
understanding of the extent to which constraint may influence future
morphological adaptation to environmental change should be one of the
key priorities of contemporary chondrichthyan evolutionary research.
There are several explanations for the lack of previous integration
between morphological and genetic studies of chondrichthyan evolution.
In the case of evo-devo studies, research effort appears to be the
primary limitations, with only a relatively low number of morphological
structures considered from a handful of species (Gillis et al., 2009).
Conducting such studies in a greater range of taxa would increase our
understanding of the genetic basis of morphological variation within
Chondrichthyes and the extent to which evolutionary constraints relating
to gene regulatory networks appear to be present (Figure 1).
Quantitative genetic studies of chondrichthyan populations have
previously been limited by the costs of genome sequencing however
technological advances are rapidly increasing the accessibility of
sequencing technologies (Mardis, 2017). The requirement of pedigree
information for quantitative trait loci (QTL) and genome wide
association studies (GWAS) also provides a limitation to their usage in
wild populations (Day-Williams et al., 2011). Recent advances have
softened this requirement, with several routes available for
quantitative genetic analyses in wild populations where pedigree
information is absent (Johnston et al., 2022). Finally, where the
genetic basis of morphological traits is known, signatures of past
selection can be detected through phylogenetic analysis (Vitti et al.,
2013). These methodologies are not mutually exclusive, and should all
contribute to future research, through which we can improve our
understanding of past morphological evolution and future ‘evolvability’
of morphological traits in chondrichthyan taxa.