Timing the developmental origins of mammalian limb diversity

Abstract

Mammals have highly diverse limbs that have contributed to their occupation of almost every niche. Researchers have long been investigating the development of these diverse limbs, with the goals of identifying developmental processes and potential biases that shape mammalian limb diversity. To date, researchers have used techniques ranging from the genomic to the anatomic to investigate the developmental processes shaping the limb morphology of mammals from five orders (Marsupialia, Chiroptera, Rodentia, Cetartiodactyla, and Perissodactyla). Results of these studies suggest that the differential expression of genes controlling diverse cellular processes underlies mammalian limb diversity. Results also suggest that the earliest development of the limb tends to be conserved among mammalian species, while later limb development tends to be more variable. This research has established the mammalian limb as a model system for evolutionary developmental biology, and set the stage for more in-depth, cross-disciplinary research into the genetic controls, tissue-level cellular behaviors, and selective pressures that have driven the developmental evolution of mammalian limbs. Ideally, these studies will be performed in a diverse suite of mammalian species within a comparative, phylogenetic framework.

Gene expression across mammalian organ development

“…As organs differentiate and mature, active genes have more restricted spatiotemporal profiles, which may reduce functional constraints and facilitate evolutionary change. The increase in species divergence as development progresses has also been described for mammalian limb development 35 and whole embryos 4–5 and we suggest it occurs in developmental systems where pleiotropy decreases as a function of time.…”

Pigeon foot feathering reveals conserved limb identity networks

“…Recent studies have characterized embryonic FL and HL bud transcriptomes in several mammalian species, including mouse, opossum, pig, and bat (Taher et al, 2011, Sears et al, 2018, Wang et al, 2018, Gyurjan et al, 2011, Eckalbar et al, 2016, Shou et al, 2005. However, similar analyses in other vertebrate classes are sparse, precluding broader comparative analyses of limb identity networks.…”

Evidence of five digits in embryonic horses and developmental stabilization of tetrapod digit number

“…A substantial body of literature in evolutionary developmental biology has focused on the question of what developmental processes are involved in regulating the diversity in the number of digits in tetrapods, with several recent major reviews on this subject [8][9][10]. Here, all published observations on early developmental stages in tetrapods with functional digits were re-examined to clarify the number of digits present at the initiation stages of autopod development.…”

“…In later stages of digit development in amniotes (post-patterning), numerous mechanisms are employed to diversify digit features: growth can be arrested, elements fused or tissue carved away by apoptosis, combined with allometric changes among digits and/or positional changes of proximal elements (e.g. [7][8][9][10]17,[24][25][26][27]. Thus, while digit reduction is a 'repeated theme in tetrapod evolution,' the number of digits at initiation is remarkably conserved and evolutionary changes in later digit development explain most of the diversity of digit patterns [10,28].…”

“…The authors recognized that the horse embryos in their comparisons were slightly older than the stage at which digit condensations initially form, likely due to very limited accessibility of early horse embryos for research. Nevertheless, this limited data on horse embryology suggested that horses only ever form three digit remnants during their development and became an important cornerstone of the general view of the evolutionary developmental biology of digits [8][9][10]. By contrast, a recent palaeontology paper proposed a novel hypothesis, based on bone articulations and ridges in fossil horses and vasculature in late foetal horses, that the identities of all five ancestral digits might be preserved in the metacarpal anatomy of the modern horse adult FL [6], but direct evidence was lacking.…”