Development, metamorphosis, morphology, and diversity: The evolution of chordate muscles and the origin of vertebrates

Abstract

Recent findings that urochordates are the closest sister-group of vertebrates have dramatically changed our understanding of chordate evolution and vertebrate origins. To continue to deepen our understanding of chordate evolution and diversity, in particular the morphological and taxonomical diversity of the vertebrate clade, one must explore the origin, development, and comparative anatomy of not only hard tissues, but also soft tissues such as muscles. Building on a recent overview of the discovery of a cardiopharyngeal field in urochordates and the profound implications for reconstructing the origin and early evolution of vertebrates, in this study we focus on the broader comparative and developmental anatomy of chordate cephalic muscles and their relation to life history, and to developmental, morphological and taxonomical diversity. We combine our recent findings on cephalochordates, urochordates, and vertebrates with a literature review and suggest that developmental changes related to metamorphosis and/or heterochrony (e.g., peramorphosis) played a crucial role in the early evolution of chordates and vertebrates. Recent studies reviewed here supported de Beer's "law of diversity" that peramorphic animals (e.g., ascidians, lampreys) are taxonomically and morphologically less diverse than nonperamorphic animals (e.g., gnathostomes), probably because their "too specialized" development and adult anatomy constrain further developmental and evolutionary innovations.

Evolutionary developmental pathology and anthropology: A new field linking development, comparative anatomy, human evolution, morphological variations and defects, and medicine

“…We were fortunate to be an active part of a recent effort, initiated by our close colleagues Julia Boughner and Campbell Rolian, to create the new field of Evolutionary Developmental Anthropology (Evo‐Devo‐Anth) (Diogo and Wood, ). In particular, our lab is developing a new subfield of Evo‐Devo‐Anth, which is designated here as Evolutionary Developmental Pathology and Anthropology, or Evo‐Devo‐P'Anth .…”

Testing the evolutionary conservation of vocal motoneurons in vertebrates

“…Similarly, the phrenic nucleus requires an extended period of Hox5 gene expression to maintain cell number and connectivity (Philippidou et al, 2012). These data, in addition to evolutionary modifications of the head, trunk, and neck region in vertebrates, suggest species-specific modifications of genetic programs play an important role in shaping the final migration, axon projection, and organization of vocal motoneurons (Bass et al, 2008; Benninger and McNeil, 2011; Cambronero and Puelles, 2000; Diogo and Ziermann, 2014; Gray, 2013; Ma et al, 2010; Piekarski and Olsson, 2007)…”

“…somatic, muscle. Nevertheless, branchial motoneurons, which include the motoneurons of cranial nerves V, VII, IX and X, are distinct from other somatic motoneurons in their developmental origin, location within the brainstem, and transcriptional profiles (Diogo and Ziermann, 2014; Gilland and Baker, 2005; Matsuoka et al, 2005; Noden and Francis‐West, 2006; Piekarski and Olsson, 2007; Tada and Kuratani, 2015). …”

Patterns of mandibular asymmetries in two types of companion rabbits

“…Paedomorphosis refers to underdevelopment, for example adults resembling a juvenile stage of its ancestor (Armbruster, Lee, Edwards, & Baldwin, ; Diogo & Ziermann, ; Goodwin, Bradshaw, & Wickens, ). It appears either when character development is delayed or through acceleration of sexual maturation (Leonova, ); paedomorphic animals require less growth to be developed as adult form (Geiger & Haussman, ; Skulachev et al, ).…”

“…Among domestic mammals, it has been described in domestic dogs (Goodwin, Levine, & McGreevy, ; Waller et al, ), which is characterized by a reduction in overall body size and retention of a juvenile head:body ratio (Goodwin et al, ), in cats (Parés‐Casanova, ; Waller et al, ), in companion rabbits (Parés‐Casanova, Sofiane, & Medina, ) and in horses (Goodwin et al, ). Gerontomorphosis or peramorphosis, on the other hand, represents a phenomenon in which animals diverge early from juvenile traits (Denoël & Joly, ; Diogo & Ziermann, ). During the last years, pet marketers have been creating a huge amount of companion rabbit phenotypes, in some cases inducing marked shifts in their development towards perceived desirable traits (Parés‐Casanova et al, ), both paedomorphic and gerontomorphic.…”