The lateral mesodermal divide: an epigenetic model of the origin of paired fins

Abstract

By examining development at the level of tissues and processes, rather than focusing on gene expression, we have formulated a general hypothesis to explain the dorso-ventral and anterior-posterior placement of paired appendage initiation sites in vertebrates. According to our model, the number and position of paired appendages are due to a commonality of embryonic tissue environments determined by the global interactions involving the two separated layers (somatic and visceral) of lateral plate mesoderm along the dorso-ventral and anterior-posterior axes of the embryo. We identify this distribution of developmental conditions, as modulated by the separation/contact of the two LPM layers and their interactions with somitic mesoderm, ectoderm, and endoderm as a dynamic developmental entity which we have termed the lateral mesodermal divide (LMD). Where the divide results in a certain tissue environment, fin bud initiation can occur. According to our hypothesis, the influence of the developing gut suppresses limb initiation along the midgut region and the ventral body wall owing to an "endodermal predominance." From an evolutionary perspective, the lack of gut regionalization in agnathans reflects the ancestral absence of these conditions, and the elaboration of the gut together with the concomitant changes to the LMD in the gnathostomes could have led to the origin of paired fins.

HoxA and HoxD expression in a variety of vertebrate body plan features reveals an ancient origin for the distal Hox program

“…Finally, it has been suggested that developing paired appendages and hindgut are associated in more ways than shared Hox expression patterns. Several key innovations following the two rounds of genome duplications in the stem lineage of vertebrates allowed for both the regionalization of the gastrointestinal tract and the emergence of paired appendages from the somatopleure in jawed vertebrates [ 51 – 53 ]. We demonstrate that HoxA DP expression is utilized to differentially pattern the distal gut, in a fashion that is reminiscent of what has been observed in the distal region of paired appendages.…”

Fishing for jaws in early vertebrate evolution: a new hypothesis of mandibular confinement

“…As for the epaxial–hypaxial differentiation, paired fins are a useful indicator. In gnathostomes, paired appendages with mesodermal contributions (muscles and endoskeleton) require ( i ) primaxial–abaxial differentiations bordered by the lateral somitic frontier and ( ii ) dorsoventral compartmentalization within the abaxial domain and in the ectoderm (Nowicki, Takimoto & Burke, ; Johanson, ; Onimaru et al ., ; Tulenko et al ., ; de la Rosa, Müller & Metscher, ). These polarities in embryonic tissues largely correspond to the adult epaxial–hypaxial distinction (epaxial: mainly derived primaxially; hypaxial: mainly derived abaxially).…”

Cranial or postcranial—Dual origin of the pectoral appendage of vertebrates combining the fin‐fold and gill‐arch theories?

“…Accordingly, in the last years various authors have postulated evolutionary models based on/supporting the fin‐fold theory. For instance, Nuno de la Rosa et al, 64 based on a developmental analysis focused on tissues and processes, proposed a model to explain the dorsoventral and anterior‐posterior placement of paired appendage initiation sites. For them, the number and position of these appendages are the result of a commonality of embryonic tissue environments determined by global interactions involving the somatic and visceral layers of lateral plate mesoderm within the embryonic dorsoventral and anterior‐posterior portion of the body.…”