The origin and evolutionary consequences of skeletal traits shaped by embryonic muscular activity, from basal theropods to modern birds

Abstract

Embryonic muscular activity (EMA) is involved in the development of several distinctive traits of birds.Modern avian diversity and the fossil record of the dinosaur-bird transition allow special insight into their evolution.Traits shaped by EMA result from mechanical forces acting at post-morphogenetic stages, such that genes often play avery indirect role. Their origin seldom suggests direct selection for the trait, but a side-effect of other changes such asmusculo-skeletal rearrangements, heterochrony in skeletal maturation, or increased incubation temperature (whichincreases EMA). EMA-shaped traits like sesamoids may be inconstant, highly conserved, or even disappear and thenreappear in evolution. Some sesamoids may become increasingly influenced in evolution by genetic-molecular mecha-nisms (genetic assimilation). There is also ample evidence of evolutionary transitions from sesamoids to bony eminencesat tendon insertion sites, and vice-versa. This can be explained by newfound similarities in the earliest development ofboth kinds of structures, which suggest these transitions are likely triggered by EMA. Other traits that require EMA fortheir formation will not necessarily undergo genetic assimilation, but still be conserved over tens and hundreds ofmillions of years, allowing evolutionary reduction and loss of other skeletal elements. Upon their origin, EMA-shapedtraits may not be directly genetic, nor immediately adaptive. Nevertheless, EMA can play a key role in evolutionaryinnovation, and have consequences for the subsequent direction of evolutionary change. Its role may be more importantand ubiquitous than currently suspected.