A novel expression domain of extradenticle underlies the evolutionary developmental origin of the chelicerate patella

Author:

Klementz Benjamin C12ORCID,Brenneis Georg3,Hinne Isaac A4,Laumer Ethan M12,Neu Sophie M12,Hareid Grace M12,Gainett Guilherme156,Setton Emily V W17,Simian Catalina8,Vrech David E8,Joyce Isabella9,Barnett Austen A9,Patel Nipam H10,Harvey Mark S11,Peretti Alfredo V8,Gulia-Nuss Monika4,Sharma Prashant P12ORCID

Affiliation:

1. Department of Integrative Biology, University of Wisconsin-Madison , Madison, Wisconsin , USA

2. University of Wisconsin-Madison Zoological Museum , Madison, Wisconsin , USA

3. Unit Integrative Zoologie, Department Evolutionsbiologie, Universität Wien , Vienna , Austria

4. Department of Biochemistry and Molecular Biology, University of Nevada , Reno, Nevada , USA

5. Department of Systems Biology, Harvard Medical School , Boston, Massachusetts , USA

6. Department of Pathology, Boston Children’s Hospital , Boston, Massachusetts , USA

7. Department of Ecology and Evolutionary Biology, Cornell University , Ithaca, New York , USA

8. Laboratorio de Biología Reproductiva y Evolución, Instituto de Diversidad y Ecología Animal (IDEA), Consejo Nacional de Investigaciones Cientifícas Técnicas (CONICET), Universidad Nacional de Córdoba , Córdoba , Argentina

9. Department of Biology, DeSales University, Center Valley , Pennsylvania , USA

10. Marine Biological Laboratory , Woods Hole, Massachusetts , USA

11. Western Australian Museum, Welshpool , Western Australia , Australia

Abstract

Abstract Neofunctionalization of duplicated gene copies is thought to be an important process underlying the origin of evolutionary novelty and provides an elegant mechanism for the origin of new phenotypic traits. One putative case where a new gene copy has been linked to a novel morphological trait is the origin of the arachnid patella, a taxonomically restricted leg segment. In spiders, the origin of this segment has been linked to the origin of the paralog dachshund-2, suggesting that a new gene facilitated the expression of a new trait. However, various arachnid groups that possess patellae do not have a copy of dachshund-2, disfavoring the direct link between gene origin and trait origin. We investigated the developmental genetic basis for patellar patterning in the harvestman Phalangium opilio, which lacks dachshund-2. Here, we show that the harvestman patella is established by a novel expression domain of the transcription factor extradenticle. Leveraging this definition of patellar identity, we surveyed targeted groups across chelicerate phylogeny to assess when this trait evolved. We show that a patellar homolog is present in Pycnogonida (sea spiders) and various arachnid orders, suggesting a single origin of the patella in the ancestor of Chelicerata. A potential loss of the patella is observed in Ixodida. Our results suggest that the modification of an ancient gene, rather than the neofunctionalization of a new gene copy, underlies the origin of the patella. Broadly, this work underscores the value of comparative data and broad taxonomic sampling when testing hypotheses in evolutionary developmental biology.

Publisher

Oxford University Press (OUP)

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