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Probing the evolution of appendage specialization by Hox gene misexpression in an emerging model crustacean.

ABSTRACT: Changes in the expression of Hox genes have been widely linked to the evolution of animal body plans, but functional demonstrations of this relationship have been impeded by the lack of suitable model organisms. A classic case study involves the repeated evolution of specialized feeding appendages, called maxillipeds, from anterior thoracic legs, in many crustacean lineages. These leg-to-maxilliped transformations correlate with the loss of Ultrabithorax (Ubx) expression from corresponding segments, which is proposed to be the underlying genetic cause. To functionally test this hypothesis, we establish tools for conditional misexpression and use these to misexpress Ubx in the crustacean Parhyale hawaiensis. Ectopic Ubx leads to homeotic transformations of anterior appendages toward more posterior thoracic fates, including maxilliped-to-leg transformations, confirming the capacity of Ubx to control thoracic (leg) versus gnathal (feeding) segmental identities. We find that maxillipeds not only are specified in the absence of Ubx, but also can develop in the presence of low/transient Ubx expression. Our findings suggest a path for the gradual evolutionary transition from thoracic legs to maxillipeds, in which stepwise changes in Hox gene expression have brought about this striking morphological and functional transformation.

SUBMITTER: Pavlopoulos A

PROVIDER: S-EPMC2728992 | biostudies-literature | 2009 Aug

REPOSITORIES: biostudies-literature

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Probing the evolution of appendage specialization by Hox gene misexpression in an emerging model crustacean.

Pavlopoulos Anastasios A Kontarakis Zacharias Z Liubicich Danielle M DM Serano Julia M JM Akam Michael M Patel Nipam H NH Averof Michalis M

Proceedings of the National Academy of Sciences of the United States of America 20090804 33

Changes in the expression of Hox genes have been widely linked to the evolution of animal body plans, but functional demonstrations of this relationship have been impeded by the lack of suitable model organisms. A classic case study involves the repeated evolution of specialized feeding appendages, called maxillipeds, from anterior thoracic legs, in many crustacean lineages. These leg-to-maxilliped transformations correlate with the loss of Ultrabithorax (Ubx) expression from corresponding segme ...[more]

PMID: 19666530

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Project description:IntroductionOnychophora is a relatively small phylum within Ecdysozoa, and is considered to be the sister group to Arthropoda. Compared to the arthropods, that have radiated into countless divergent forms, the onychophoran body plan is overall comparably simple and does not display much in-phylum variation. An important component of arthropod morphological diversity consists of variation of tagmosis, i.e. the grouping of segments into functional units (tagmata), and this in turn is correlated with differences in expression patterns of the Hox genes. How these genes are expressed in the simpler onychophorans, the subject of this paper, would therefore be of interest in understanding their subsequent evolution in the arthropods, especially if an argument can be made for the onychophoran system broadly reflecting the ancestral state in the arthropods.ResultsThe sequences and embryonic expression patterns of the complete set of ten Hox genes of an onychophoran (Euperipatoides kanangrensis) are described for the first time. We find that they are all expressed in characteristic patterns that suggest a function as classical Hox genes. The onychophoran Hox genes obey spatial colinearity, and with the exception of Ultrabithorax (Ubx), they all have different and distinct anterior expression borders. Notably, Ubx transcripts form a posterior to anterior gradient in the onychophoran trunk. Expression of all onychophoran Hox genes extends continuously from their anterior border to the rear end of the embryo.ConclusionsThe spatial expression pattern of the onychophoran Hox genes may contribute to a combinatorial Hox code that is involved in giving each segment its identity. This patterning of segments in the uniform trunk, however, apparently predates the evolution of distinct segmental differences in external morphology seen in arthropods. The gradient-like expression of Ubx may give posterior segments their specific identity, even though they otherwise express the same set of Hox genes. We suggest that the confined domains of Hox gene expression seen in arthropods evolved from an ancestral onychophoran-like Hox gene pattern. Reconstruction of the ancestral arthropod Hox pattern and comparison with the patterns in the different arthropod classes reveals phylogenetic support for Mandibulata and Tetraconata, but not Myriochelata and Atelocerata.

Dataset Information

Probing the evolution of appendage specialization by Hox gene misexpression in an emerging model crustacean.

Publications

Probing the evolution of appendage specialization by Hox gene misexpression in an emerging model crustacean.

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