Expression of Hox, Cdx, and Six3/6 genes in the hoplonemertean Pantinonemertes californiensis offers insight into the evolution of maximally indirect development in the phylum Nemertea

EvoDevo

Svetlana A Maslakova¹  Laurel S Hiebert¹ 

[1] Oregon Institute of Marine Biology, University of Oregon, Charleston, OR, USA

关键词: Hox;    Larval evolution;    Nemertea;    Pilidium;    Maximally indirect development;   

Others  :  1222380
DOI  :  10.1186/s13227-015-0021-7

 received in 2015-02-05, accepted in 2015-07-15,  发布年份 2015

【 摘 要 】

Background

Maximally indirect development via a pilidium larva is unique to the pilidiophoran clade of phylum Nemertea. All other nemerteans have more or less direct development. The origin of pilidial development with disjunct invaginated juvenile rudiments and catastrophic metamorphosis remains poorly understood. While basal members of the phylum, the Palaeonemertea, do not appear to have ever had a pilidium, certain similarity exists in the development of the Pilidiophora and the sister clade, the Hoplonemertea. It is unclear whether this similarity represents the homology and whether pilidial development evolved before or after pilidiophorans diverged from hoplonemerteans. To gain insight into these questions, we examined the expression of Hox, Cdx, and Six3/6 genes in the development of the hoplonemertean Pantinonemertes californiensis and expression of Six3/6 in the pilidium of Micrura alaskensis. To further characterize the function of larval structures showing expression of these genes, we examined the serotonergic nervous system and cell proliferation in P. californiensis.

Results

We show that Hox and Cdx genes, which pattern the pilidial imaginal discs giving rise to the juvenile trunk, are expressed in paired posterior epidermal invaginations in P. californiensis larvae. We also show that Six3/6 patterns both the pilidial cephalic discs, which give rise to the juvenile head, and a pair of anterior epidermal invaginations in hoplonemertean development. We show that anterior invaginations in larval P. californiensis are associated with a pair of serotonergic neurons, and thus may have a role in the development of the juvenile nervous system. This is similar to the role of cephalic discs in pilidiophoran development. Finally, we show that four zones of high cell proliferation correspond to the paired invaginations in P. californiensis, suggesting that these invaginations may play a similar role in the development of the hoplonemertean juvenile to the role of imaginal discs in the pilidium, which also exhibit high rates of cell proliferation.

Conclusions

Expression of Hox, Cdx, and Six3/6 genes supports the homology between the imaginal discs of the pilidium and the paired larval invaginations in hoplonemerteans. This suggests that invaginated juvenile rudiments (possible precursors to pilidial imaginal discs) may have been present in the most recent common ancestor of the Pilidiophora and Hoplonemertea.

【 授权许可】

   
2015 Hiebert and Maslakova.

【 图 表 】

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