MBE Advance Access published online on September 26, 2008
Molecular Biology and Evolution, doi:10.1093/molbev/msn203
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Research Article |
Evolution of Soldier-Specific Venomous Protease in Social Aphids
1 Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan
2 Division of Natural Sciences, The Open University of Japan, Chiba 261-8586, Japan
3 Department of System Sciences (Biology), University of Tokyo, Tokyo 153-8902, Japan
4 INRA, UMR1099 BIO3P, F-35653 Le Rheu, France
Address for correspondence and reprints: Takema Fukatsu, Institute for Biological Resources and Functions, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba 305-8566, Japan. E-mail: t-fukatsu{at}aist.go.jp
Received for publication May 7, 2008. Revision received June 25, 2008. Revision received August 7, 2008. Accepted for publication September 9, 2008.
In social aphids of the genus Tuberaphis, a cysteine protease gene of the family cathepsin B exhibits soldier-specific expression and intestinal protease production. The product is orally excreted and injected by soldier nymphs into natural enemies, thereby exerting an insecticidal activity. In an attempt to gain insights into when and how the novel venomous protease for the altruistic caste has evolved, we investigated the soldier-specific type (S-type) and non-specific type (N-type) cathepsin B genes from social and non-social aphids. All the social aphids examined, representing the genera Tuberaphis, Astegopteryx and Cerataphis, possessed both the S-type and N-type genes. Phylogenetically distant non-social aphids also possessed cathepsin B genes allied to the S-type and the N-type, indicating the evolutionary origin of these genes in the common ancestor of extant aphids. In Tuberaphis species, the S-type genes exhibited significant soldier-specific expression and accelerated molecular evolution, whereas the N-type genes did not. In Astegopteryx and Cerataphis species, meanwhile, both the S-type and N-type genes exhibited neither remarkable soldier-specific expression nor accelerated molecular evolution. These results suggest that the S-type gene acquired the soldier-specific expression and the venom function after divergence of the genus Tuberaphis. On the structural model of the S-type protease of T. styraci, the accelerated molecular evolution was associated with the molecular surface rather than the catalytic cleft, suggesting that the venom activity was probably acquired by relatively minor modifications on the molecular surface rather than by generation of a novel active site. In C. jamuritsu, the S-type gene was, although containing a stop codon, structurally almost intact and still transcribed, suggesting recent pseudogenization of the gene copy and possible relevance to relaxed functional constraint in the highly multiplied protease gene family. On the basis of these results, we suggest that the massive amplification in aphid cathepsin B genes might have predisposed the evolution of venomous protease in the social aphid lineage, and argue that gene duplication, accelerated molecular evolution and acquisition of novel gene function must have played considerable roles in the evolution of complex biological systems including insect sociality.
Key Words: social aphid • soldier caste • venom protein • cathepsin B protease • accelerated evolution • gene duplication