Staggered Hox expression is more widespread among molluscs than previously appreciated

Abstract

Hox genes are expressed along the anterior–posterior body axis in a colinear fashion in the majority of bilaterians. Contrary to polyplacophorans, a group of aculiferan molluscs with conserved ancestral molluscan features, gastropods and cephalopods deviate from this pattern by expressing Hox genes in distinct morphological structures and not in a staggered fashion. Among conchiferans, scaphopods exhibit many similarities with gastropods, cephalopods and bivalves, however, the molecular developmental underpinnings of these similar traits remain unknown. We investigated Hox gene expression in developmental stages of the scaphopod Antalis entalis to elucidate whether these genes are involved in patterning morphological traits shared by their kin conchiferans. Scaphopod Hox genes are predominantly expressed in the foot and mantle but also in the central nervous system. Surprisingly, the scaphopod mid-stage trochophore exhibits a near-to staggered expression of all nine Hox genes identified. Temporal colinearity was not found and early-stage and late-stage trochophores, as well as postmetamorphic individuals, do not show any apparent traces of staggered expression. In these stages, Hox genes are expressed in distinct morphological structures such as the cerebral and pedal ganglia and in the shell field of early-stage trochophores. Interestingly, a re-evaluation of previously published data on early-stage cephalopod embryos and of the gastropod pre-torsional veliger shows that these developmental stages exhibit traces of staggered Hox expression. Considering our results and all gene expression and genomic data available for molluscs as well as other bilaterians, we suggest a last common molluscan ancestor with colinear Hox expression in predominantly ectodermal tissues along the anterior–posterior axis. Subsequently, certain Hox genes have been co-opted into the patterning process of distinct structures (apical organ or prototroch) in conchiferans.

Hox gene expression during development of the phoronid Phoronopsis harmeri

“…Although Hox genes in Bilateria are predominantly expressed in the ectoderm (including nervous system) and their ectodermal expression is often considered as an ancestral feature [14,28,34], in various spiralian species certain Hox genes are also expressed in mesoderm, endoderm and clade-specific structures like chaetal sacs or shell fields (e.g. [16,23,24,27,29,31,35,36,[39][40][41]46]; Table 1). Inclusion of the data on Hox expression in Phoronida gives some new insight into the understanding of the evolution of germ layerspecific Hox expression in Spiralia.…”

“…On the other hand, in animals with non-catastrophic metamorphosis (e.g. cephalochordates, mollusks, annelids or brachiopods), the Hox genes seem to pattern both the larval and adult body plans in a relatively similar way [31,39,40,46,48]. However, studies focusing on metamorphosis-related differences of Hox gene expression in Bilateria are still limited to a relatively few evolutionary lineages [40,91].…”

Learning from beautiful monsters: phylogenetic and morphogenetic implications of left-right asymmetry in ammonoid shells

“…More generally, the wide morphological diversity observed in modern mollusks has long been thought to be explained by differences in Hox gene interactions and expressions or changes in their downstream genes (e.g., [63]). Yet, all available evidence so far suggests that Hox genes are not expressed in the larval mantle of recent cephalopods [64,65], contrarily to all other clades of mollusks. Clearly, these important questions require more investigation.…”

Hox gene expression during the development of the phoronidPhoronopsis harmeri

“…On the other hand, in animals with more gradual metamorphosis (e.g. cephalochordates, mollusks, annelids or brachiopods), the Hox genes seem to pattern both the larval and adult body plans in a relatively similar way (31,39,40,46,48). However, studies focusing on metamorphosis-related differences of Hox gene expression in Bilateria are still limited to a relatively few evolutionary lineages (40,92).…”

“…nervous system) and their ectodermal expression is often considered as an ancestral feature(14,28,34), in various spiralian species certain Hox genes are also expressed in mesoderm, endoderm and clade-specific structures like chaetal sacs or shell fields (e.g (16,23,24,27,29,31,35,36,(39)(40)(41)46)…”