The importance of cartilage to amphibian development and evolution

Abstract

The duality of amphibians is epitomized by their pharyngeal arch skeletons, the larval and adult morphologies of which enable very different feeding and breathing behaviors in aquatic and terrestrial life. To accomplish this duality, amphibian pharyngeal arch skeletons undergo two periods of patterning: embryogenesis and metamorphosis, and two periods of growth: larval and postmetamorphic. Their extreme ontogenetic variation, however, is coupled with relatively limited phylogenetic variation. I propose that amphibians face an evolutionary tradeoff between their ontogenetic and phylogenetic diversification that stems from the need to grow and transform the pharyngeal arch skeleton in cartilage rather than bone. Cartilage differs fundamentally from bone in its histology, function, development and growth. Cartilage is also the first skeletal tissue to form embryonically and provides more cellular pathways for shape change than bone. This article combines morphological, histological and experimental perspectives to explore how pharyngeal arch cartilage shape is controlled in amphibian embryogenesis, growth and metamorphosis, and how amphibian skeletal ontogenies are impacted by using cartilage to evolve a complex life cycle and in evolving away from a complex life cycle.

Evolutionary repression of chondrogenic genes in the vertebrate osteoblast

“…Therefore, any meaningful discussion about skeletal cell evolution needs to include all of the major vertebrate classes (Fig. 3), and despite some recent work, amphibians remain overlooked [3,[26][27][28][33][34][35][36][37][38][39][40][41][42][43][44][45][46][47][48] .…”

Amphibian Hormones, Calcium Physiology, Bone Weight, and Lung Use Call for a More Inclusive Approach to Understanding Ossification Sequence Evolution

“…The period of transformation is also one of high vulnerability and mortality, implying there is strong selection to keep the changes as brief and as coordinated as possible (Wassersug and Sperry, 1977;Wassersug and Hoff, 1982). That many bones appear outside of this period, that almost all bone rudiments develop directly to their adult size and shape (Figure 1)-only the salamander vomer and coronoid attain shapes designed specifically for larval functions-and that the major functional transformations at metamorphosis are effected more in cartilage than in bone underscores the primacy of cartilage in the origin and diversification of amphibian metamorphosis (Rose, 2014b). These points also accentuate the conclusion drawn from other vertebrates that timing of bone appearance is not strongly tied to, and therefore not predictive of, onset of bone function in load bearing (Mabee and Trendler, 1996;Maxwell, 2008;Maxwell and Larsson, 2009).…”

“…There has been ample research on how bone and cartilage growth is affected by mechanical stress for mammals and birds (Murray, 1936;Herring, 1993;Hall, 2005), but relatively little for anamniotes, especially ones with biphasic development. We are beginning to understand the cellular mechanisms that regulate skeletal shape during growth (Vandenberg et al, 2012;Rose, 2014b;Kaucka et al, 2017;Pinet et al, 2019) and that produce interspecific differences in long bone (Farnum et al, 2008;Cooper et al, 2013) and dermal bone shapes (Slater et al, 2009). We have yet to investigate how plasticity in skeletal growth is regulated by the environmental, behavioral, and physiological factors discussed here and elsewhere (Aubret and Shine, 2009;Serrat, 2014).…”

Metamorphosis imposes variable constraints on genome expansion through effects on development

“…In direct-developing species, the larval growth stage is eliminated, and embryogenesis and metamorphosis are integrated into a single sequence of developmental events that takes place inside the egg (Alberch 1989; Rose 2014). This entire sequence must be fueled by yolk provisioned by the mother.…”