The evolution of bilaterian body-plan: perspectives from the developmental genetics of the Acoela (Aeoelomorpha).

Abstract

The mesoderm is the third germ layer, which is formed at gastrulation between the endoderm and the ectoderm in triploblastsc animals (Bilateria).

The mesoderm differentiates into muscles, connective tissues and coelomic cavities. These structures have been key evolutionary innovations that prompted the enormous radiation of the bilaterians that at present make up for the 90% of animal species. As such, understanding the evolution of the mesoderm and its derivatives it is pivotal to understand the evolution of animals.

In this thesis I have characterized the molecular patterning of the mesoderm and its derivatives (mainly muscles) in two different acoel species: Symsagittifera roscoffensis and Isodiametra pulchra.

The acoels belong to the phylum Acoelomorpha (togheter with nemertodermatids and Xenoturbella). The phylogenetic placement of the Acoelomorpha is highly debated between a position basal to the bilaterians or nested inside the deuterostomes.

The Acoelomorpha are morphologically simple animals and a trait sometimes considered a direct link to the cnidarians, the Bilateria sister group. With them they the acoelomorphs share a blind gut and a non centralized nervous system. Within the acoelomorphs, the acoels present the most derived body plan, however it is still rather simple if compared to other bilaterians. The nervous system for example is condensed anteriorly but not clear dorso ventral centralization exists as in most of the remaining bilaterians (the nerve cords are distributed circumferentially around the body). The mesoderm only develops from endodermal precursors, and this might be ancestral, since it is thought that the mesoderm evolved from the endoderm of a diploblastic, cnidarian-like ancestor.

The muscles are the only mesodermal derivative in most basal acoelomorphs taxa, although in more advanced ones a parenchymal tissue, stem cells, and gonads also occupy the mesodermal space. The embryonic origins of the latter though, are at present still unknown. Thus acoelomorphs present most of traits considered to be eumetazoan ancestral traits (i.e. most of traits are also part of the cnidarians ground pattern), but still that the possibility that their body plan evolved in consequence of a secondary reduction must be considered as they could be more related to other deuterostomes than cnidarians.

I have first investigated the molecular architecture of the muscles in the acoel Symsagittifera roscoffensis and found that although they have a smooth ultrastructural aspect they are molecularly more similar to the bilaterian striated muscles given that tey express key genes that control the contraction in the striated cells. This could be considered a first step into the evolution of the striated musculature without fully reaching it. Indeed, cnidarians have smooth epithelio muscular cells likely regulated by the same bilaterian smooth muscle proteins. However, the possibility of a secondary loss of the striation pattern cannot be discarded given that this already happened in some other bilaterians. Second, I have analyzed the expression of bilaterian mesodermal genes during embryogenesis and postembryonic development of Isodiametra pulchra and found that all but one (a FoxA ortholog) are expressed at the anterior pole, the site where the first myocytes start to differentiate. In juveniles and adults these genes are all expressed in muscles or at least a subset of them. Moreover the same genes are expressed in the gonads of I. pulchra and therefore it suggests that they could orginate in the endo-mesoderm of the worm. The cnidarians orthologues of these genes are expressed in the endoderm, which is moreover the site of the gametes differentation. The similarity between cnidarians endoderm and acoels mesoderm are astonishing, however before drawing conclusions we need a solid phylogenetic frame.

Los acelos son unos gusanos, principalmente marinos, de simetría bilateral y aplastados según el eje dorso ventral, que pertenecen al grupo de los acelomorfos (acelos +nemertodermatidos+xenoturbellidos), cuya posición filogenética es tema de debate entre los biólogos evolucionistas.

Los acelomorfos carecen de cavidades corporales, su sistema digestivo es ciego y su sistema nervioso consiste de una concentración neuronal anterior y cuerda nerviosas no claramente desplazadas hacía el lado dorsal o ventral.

La simplicidad morfológica de los acelos, entremedia entre la de cnidarios y bilaterales superiores, les hace buenos candidatos para el estudio de la transición de animales radiales-diploblastos a bilaterales-triploblastos.

En esta tesis se presentan datos sobre el desarrollo e la especificación molecular del mesodermo, que ha sido una de las innovaciones claves para la radiación de los bilaterales.

S. roscoffensis que como todos los acelos tiene exclusivamente musculatura de tipo liso, expresa un gen ortólogo a la troponina, un proteína clave para la regulación de los músculos estriados, y que no existe en cnidarios. La explicación más parsimoniosa es que las bases moleculares de evolución de músculos estriados se han implantado en los acelos, aunque estos no hayan alcanzado la condición completa (explicación favorecida si los acelomorfos son confirmados como grupo hermano de los demás bilaterales). Por otra parte se puede considerar esta condición como debida a una reducción secundaria (explicación favorecida en el caso que los acelos se confirmen ser deuteróstomos).

Los ortólogos de genes endodermales de cnidarios y con clara expresión mesodermal en bilaterales se expresan en la músculatura del acelo l. pulchra. Estos datos concuerdan perfectamente con la evolución del mesodermo a partir del endodermo de animales diploblásticos. Aun así, es difícil proponer un modelo específico de evolución de miocitos hasta que la posición filogenética de los acelomorfos no esté resuelta.