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.