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. 2024 Mar 6;14(3):jkad299.
doi: 10.1093/g3journal/jkad299.

A comprehensive evolutionary scenario for the origin and neofunctionalization of the Drosophila speciation gene Odysseus (OdsH)

William Vilas Boas Nunes  1   2 , Daniel Siqueira Oliveira  1   2 , Guilherme de Rezende Dias  3 , Antonio Bernardo Carvalho  3 , Ícaro Putinhon Caruso  1 , Joice Matos Biselli  1 , Nathalie Guegen  4 , Abdou Akkouche  4 , Nelly Burlet  2 , Cristina Vieira  2 , Claudia M A Carareto  1
Affiliations

A comprehensive evolutionary scenario for the origin and neofunctionalization of the Drosophila speciation gene Odysseus (OdsH)

William Vilas Boas Nunes et al. G3 (Bethesda). .

Abstract

Odysseus (OdsH) was the first speciation gene described in Drosophila related to hybrid sterility in offspring of mating between Drosophila mauritiana and Drosophila simulans. Its origin is attributed to the duplication of the gene unc-4 in the subgenus Sophophora. By using a much larger sample of Drosophilidae species, we showed that contrary to what has been previously proposed, OdsH origin occurred 62 MYA. Evolutionary rates, expression, and transcription factor-binding sites of OdsH evidence that it may have rapidly experienced neofunctionalization in male sexual functions. Furthermore, the analysis of the OdsH peptide allowed the identification of mutations of D. mauritiana that could result in incompatibility in hybrids. In order to find if OdsH could be related to hybrid sterility, beyond Sophophora, we explored the expression of OdsH in Drosophila arizonae and Drosophila mojavensis, a pair of sister species with incomplete reproductive isolation. Our data indicated that OdsH expression is not atypical in their male-sterile hybrids. In conclusion, we have proposed that the origin of OdsH occurred earlier than previously proposed, followed by neofunctionalization. Our results also suggested that its role as a speciation gene might be restricted to D. mauritiana and D. simulans.

Keywords: OdsH expression; unc-4; Drosophilidae; gene duplication; homeodomain; transcription factor.

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Conflict of interest statement

Conflicts of interest The authors declare no conflicts of interest.

Figures

Fig. 1.
Fig. 1.
Relative positions of gene sequences in the neighborhood of OdsH and unc-4 in Drosophilinae genomes. The representation of the phylogenetic relationships is based on Suvorov et al. (2022).
Fig. 2.
Fig. 2.
Gene structure of unc-4 and OdsH in Drosophilinae. An asterisk denotes present only in D. ananassae, D. virilis, and D. grimshawi. A double asterisk denotes present only in D. arizonae, D. mojavensis, and S. lebanonensis.
Fig. 3.
Fig. 3.
Calibrated Bayesian phylogenetic inference of the sequences of the paralog genes unc-4 and OdsH using the GTR+G+I substitution model. The analysis was performed with 405 nucleotide sites from 162 sequences. All positions containing gaps and ambiguous bases were removed from the pairwise sequence analysis. The branches referring to the Drosophila taxonomic groups were compressed. At the root of each clade, the PP is presented by black (darker) (>0.9) and gray (lighter) (>0.7) circles, and the estimated times of divergence are indicated. The analysis was conducted in BEAST v16.1. The unc-4 clade (green), subdivided into the more basal single-copy Steganinae (outgroup—black) and Drosophilinae, is presented at the base of the phylogeny followed by the OdsH clade in the upper part (pink). Monophyletic taxonomic groups of the Drosophila genus were compressed. Uncompressed clades can be seen in Supplementary Fig. 7. Subgenera are highlighted in blue (Sophophora) and yellow (Drosophila).
Fig. 4.
Fig. 4.
Enriched TFBSs in the regulatory sequence of unc-4 and OdsH. a) TFBS enrichment values for OdsH (red) and unc-4 (blue). Gray dots represent transcription factors whose binding sites did not differ from each other. b) Differentially present enriched TFBS between sister hybridizing species.
Fig. 5.
Fig. 5.
Functional motifs in Unc-4 and OdsH proteins. a) Representations of the Unc-4 and OdsH primary structures in D. melanogaster and functional motifs found in Drosophilinae: homeodomain (blue) and octapeptide (red). b) 3D models of Unc-4 and OdsH homeodomains. The N-terminal tail is presented in blue, and the C-terminal tail is presented in red. c) Total energy variation of the OdsH and DNA homeodomain complex, by species, in relation to Unc-4. d) Energy variation of the OdsH and DNA homeodomain complex, per substitution, relative to Unc-4, by species along the amino acid chain (0–54). Sites without a gray circle represent replacement in all analyzed species. The boxes represent the positions of the 3 α-helices. Overlapping dots represent shared mutations: 5—D. mojavensis, D. virilis, and D. grimshawi; 5—D. persimilis and D. pseudoobscura; 17—melanogaster complex; 17—D. persimilis, D. pseudoobscura, D. ananassae, D. mojavensis, and D. virilis; 18—D. sechellia and D. simulans; 18—D. persimilis, D. pseudoobscura, D. mojavensis, D. virilis, and D. grimshawi; 19—D. simulans, D. mauritiana, D. yakuba, and D. ananassae; 32—melanogaster complex; 37—D. melanogaster, D. sechellia, and D. mauritiana; 39—all except D. simulans, D. sechellia, and D. mauritiana; and 52—all species.
Fig. 6.
Fig. 6.
smRNA FISH of OdsH in the testes of D. arizonae, D. mojavensis baja, and its hybrids. a) Scheme of Drosophila spermatogenesis, based on Witt et al. (2019). b) Panorama of testes of D. mojavensis baja. c) Panorama of the testes of D. arizonae. d) Apical region of the testis of D. mojavensis baja. e) Apical region of the testis of D. mojavensis baja. f) Apical region of the H♀mojbaja♂ari (fertile) testis. g) Apical region of the H♀ari♂mojbaja (sterile) testis. Notes—blue: DAPI; red: OdsH probes. H, hybrid.
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