Conserved Mechanisms, Novel Anatomies: The Developmental Basis of Fin Evolution and the Origin of Limbs

Abstract

The transformation of paired fins into tetrapod limbs is one of the most intensively scrutinized events in animal evolution. Early anatomical and embryological datasets identified distinctive morphological regions within the appendage and posed hypotheses about how the loss, gain, and transformation of these regions could explain the observed patterns of both extant and fossil appendage diversity. These hypotheses have been put to the test by our growing understanding of patterning mechanisms that regulate formation of the appendage axes, comparisons of gene expression data from an array of phylogenetically informative taxa, and increasingly sophisticated and elegant experiments leveraging the latest molecular approaches. Together, these data demonstrate the remarkable conservation of developmental mechanisms, even across phylogenetically and morphologically disparate taxa, as well as raising new questions about the way we view homology, evolutionary novelty, and the often non-linear connection between morphology and gene expression. In this review, we present historical hypotheses regarding paired fin evolution and limb origins, summarize key aspects of central appendage patterning mechanisms in model and non-model species, address how modern comparative developmental data interface with our understanding of appendage anatomy, and highlight new approaches that promise to provide new insight into these well-traveled questions.

Paired fins in vertebrate evolution and ontogeny

“…At the base of the teleost fin, only the pro‐ and mesopterygium and the radialia remain, or, according to some researchers, only the radialia, which in turn are divided into proximal and distal elements (Enny et al, 2020; Yano et al, 2012). The fin blade of teleosts is mainly formed by highly developed exoskeletal rays—lepidotrichia—which have no homologues in terrestrial vertebrates (Cass et al, 2021; Yano et al, 2012). In contrast, in lobe‐finned fishes (Sarcopterygii) the propterygium and mesopterygium are reduced and the metapterygium grows, becomes segmented and sometimes very long, giving rise to a rope‐like fin, e.g.…”

New insights into Xenopus sex chromosome genomics from the Marsabit clawed frog X. borealis

“…However, sex chromosomes of other groups such as squamate reptiles (Gamble et al, 2015; Pennell et al, 2018), teleost fish (Pennell et al, 2018) and amphibians (Evans et al, 2012; Jeffries et al, 2018; Ma & Veltsos, 2021; Pennell et al, 2018) change frequently; some—and perhaps many—of these changes are also associated with origins of novel triggers for sex determination. This contrasts sharply with highly conserved developmental control of several other traits such eyes (Onuma et al, 2002), limbs (Cass et al, 2021) and non‐gonadal organs (Irie & Kuratani, 2011), raising the question of why there is such diversity in the genetic basis of sex determination (Bachtrog et al, 2014; Palmer et al, 2019).…”

“…change frequently; some-and perhaps many-of these changes are also associated with origins of novel triggers for sex determination. This contrasts sharply with highly conserved developmental control of several other traits such eyes (Onuma et al, 2002), limbs (Cass et al, 2021) and non-gonadal organs (Irie & Kuratani, 2011), raising the question of why there is such diversity in the genetic basis of sex determination (Bachtrog et al, 2014;Palmer et al, 2019).…”

Organization of the body wall in lampreys informs the evolution of the vertebrate paired appendages

“…One of the major anatomical differences between them is that only gnathostomes generate bones. Paired appendages are a unique feature of gnathostomes, which are formed during embryogenesis by contributions from the ectoderm, paraxial mesoderm, and lateral plate mesoderm (Cass et al, 2021; Gilbert, 2016; Nakamura et al, 2021). The lateral plate mesoderm is a layered structure that gives rise to a variety of cell types including the heart, smooth muscles, blood, and fin/limb skeletons (Figure 1a; Prummel et al, 2020).…”