Limb-Bone Development of Seymouriamorphs: Implications for the Evolution of Growth Strategy in Stem Amniotes

Jordi Estefa,Jozef Klembara,Paul Tafforeau,Sophie Sanchez

doi:10.3389/feart.2020.00097

Abstract

Tetrapod life on land was the result of a lengthy process, the final steps of which resulted in full independence of amniotic tetrapods from the aquatic environment. Developmental strategies, including growth rate and the attainment of sexual maturity, played a major role in this transition. Early amniotes, such as Ophiacodon, tended to reach sexual maturity in a year while most non-amniotic Paleozoic tetrapods (including Devonian tetrapods and temnospondyls) became adult after 3 to 11 years. This ontogenetic transition is accompanied by a drastic change in growth rate and bone microstructure suggesting faster growth dynamics in early amniotes than in Devonian tetrapods and temnospondyls. Was the acquisition of a faster development (earlier sexual maturity and faster growth rate) a drastic evolutionary event or an extended process over geological time? To answer this question, the limb bone histology of two Early Permian (i.e. 270-290 million-year-old) stem-amniote seymouriamorphs, Seymouria sanjuanensis and Discosauriscus austriacus, were investigated. We used three-dimensional bone paleohistology based on propagation phase-contrast synchrotron microtomography. Both seymouriamorphs display relatively fast bone growth and dynamics (even though cyclic in the humerus of D. austriacus). This significantly contrasts with the slow primary bone deposition encountered in the stylopods of temnospondyls and Devonian (i.e. 360 million-year-old) stem tetrapods of similar sizes. On the basis of skeletochronological data, the seymouriamorph D. austriacus retained a long pre-reproductive period as observed in Devonian tetrapods and most temnospondyls. The combination of characteristics (faster growth rate but long pre-reproductive period) suggests that the shift towards an amniotic developmental strategy was an extended process in the evolutionary history of amniotes.

Highlights

Amniotes were the first animals in the evolutionary history of vertebrates to become independent from the aquatic environment (Sumida and Martin, 1997; Sander, 2012)
Histological investigations demonstrated that Devonian (i.e., 380–360 million-year-old) stem tetrapods had a slow development with a late onset of sexual maturity and a slow growth rate (Sanchez et al, 2014, 2016; Kamska et al, 2019) compared to early amniotes of the same size (e.g., Ophiacodon, Laurin and de Buffrénil, 2016)
Conclusion on Seymouriamorphs These 3D observations on both S. sanjuanensis and D. austriacus suggest that seymouriamorphs had a faster humeral growth than previously suggested (Sanchez et al, 2008)

Summary

Introduction

Amniotes were the first animals in the evolutionary history of vertebrates to become independent from the aquatic environment (Sumida and Martin, 1997; Sander, 2012) This ecological transition resulted in the evolution of an amniotic egg (Reisz, 1997; Piñeiro et al, 2012) but significantly affected the life history traits of amniotes, including reproductive strategies (i.e., live-bearing versus egg lay-down, Piñeiro et al, 2012; Sander, 2012; egg number and size, Duellman and Trueb, 1994; parental care, Crump, 1996; Botha-Brink and Modesto, 2007; Rafferty and Reina, 2012), skeletal maturity and growth rate (Sanchez et al, 2008). In order to investigate this shift in skeletal development and bone dynamics, we decided to focus on seymouriamorphs, considered by most authors as stem amniotes (e.g., Anderson, 2007, 2008; Ruta and Coates, 2007; Sigurdsen and Green, 2011; Pardo et al, 2017a – even though a diverging opinion has been published, Vallin and Laurin, 2004; Marjanovicand Laurin, 2013 – see phylogenetic considerations in Section “Materials and Methods”)

Methods

Results

Discussion

Conclusion