Frequent nonrandom shifts in the temporal sequence of developmental landmark events during teleost evolutionary diversification

Abstract

Morphological transformations can be generated by evolutionary changes in the sequence of developmental events. In this study, we examined the evolutionary dynamics of the developmental sequence on a macroevolutionary scale in teleosts. Using the information from previous reports describing the development of 31 species, we extracted the developmental sequences of 19 landmark events involving the formation of phylogenetically conserved body parts; we then inferred ancestral developmental sequences by two different parsimony‐based methods—event‐pairing and continuous analysis. The phylogenetic comparisons of these sequences revealed event‐dependent heterogeneity in the frequency of sequence changes. Most of the sequence changes occurred as exchanges of temporally neighboring events. These heterochronic changes in developmental sequences accumulated along evolutionary time, but the precise distribution of the changes over the teleostean phylogeny remains unclear due to technical limitations.

Normal stages of embryonic development of a brood parasite, the rosy bitterling Rhodeus ocellatus (Teleostei: Cypriniformes)

“…We have described 24 stages in the development of the rosy bitterling using microCT and have made the stages comparable to the Kimmel stages for the zebrafish. These corresponding developmental stage series laying the foundation for our subsequent research, a comparison of the sequence of developmental events with sequences in other non‐parasitism teleost based on parsimony analysis (Ito et al, 2019; Jeffery et al, 2005). Sequence heterochrony (changes in the order in which events occur) is an important mechanism for the evolution of development (Bininda‐Emonds et al, 2002; Mabee et al, 2000).…”

Developmental bias, macroevolution, and the fossil record

“…and different modes of developmental change may actually be more frequent. In contrast, sequence heterochronies are well-documented (e.g., Bininda-Emonds, Jeffery, & Richardson, 2003;Bininda-Emonds, Jeffery, Coates, & Richardson, 2002;Carril & Tambussi, 2017;Ito, Matsumoto, & Hirata, 2019;Koyabu et al, 2014;K. Local heterochrony is often manifest postembryonically and so can often be detected paleontologically (see examples in Jablonski, 2017a;Urdy, Wilson, Haug, & Sánchez-Villagra, 2013), and some have occurred repeatedly.…”

“…For example, local paedomorphic reduction of ambulacral rows in echinoderms was evidently instrumental in the origin of many of the peculiar body plans of the early Paleozoic by providing an easy means of altering feeding and respiratory structures (Sumrall & Wray, ). In contrast, sequence heterochronies are well‐documented (e.g., Bininda‐Emonds, Jeffery, & Richardson, ; Bininda‐Emonds, Jeffery, Coates, & Richardson, ; Carril & Tambussi, ; Ito, Matsumoto, & Hirata, ; Koyabu et al, ; K. K. Smith, ), but are most often embryonic and so are difficult to detect paleontologically. Nonetheless, macroevolutionary consequences can still be evaluated in a comparative framework when changes in the sequence of developmental events can be pinpointed phylogenetically.…”