Parallel Losses of Blue Opsin Correlate with Compensatory Neofunctionalization of UV-Opsin Gene Duplicates in Aphids and Planthoppers

SIMPLE SUMMARY: Hemiptera is one of the largest and most diverse insect orders, yet our knowledge about visual opsin evolution in this group remains preliminary. This study provides an updated survey of visual opsin genes in the Hemiptera, which reveals that the subfamily of blue-sensitive opsin receptor genes has been independently lost in planthoppers and aphids. Moreover, in both groups, tandem duplication of UV-sensitive opsins produced sister paralogs that diverged by maintaining ancestral UV sensitivity versus shifting to blue sensitivity and thereby likely compensating for the loss of the blue-sensitive opsin subfamily. The study further shows that these parallel trajectories at the level of gene family evolution are associated with mostly convergent changes at the level of protein sequence evolution. ABSTRACT: Expanding on previous efforts to survey the visual opsin repertoires of the Hemiptera, this study confirms that homologs of the UV- and LW-opsin subfamilies are conserved in all Hemiptera, while the B-opsin subfamily is missing from the Heteroptera and subgroups of the Sternorrhyncha and Auchenorrhyncha, i.e., aphids (Aphidoidea) and planthoppers (Fulgoroidea), respectively. Unlike in the Heteroptera, which are characterized by multiple independent expansions of the LW-opsin subfamily, the lack of B-opsin correlates with the presence of tandem-duplicated UV-opsins in aphids and planthoppers. Available data on organismal wavelength sensitivities and retinal gene expression patterns lead to the conclusion that, in both groups, one UV-opsin paralog shifted from ancestral UV peak sensitivity to derived blue sensitivity, likely compensating for the lost B-opsin. Two parallel bona fide tuning site substitutions compare to 18 non-corresponding amino acid replacements in the blue-shifted UV-opsin paralogs of aphids and planthoppers. Most notably, while the aphid blue-shifted UV-opsin clade is characterized by a replacement substitution at one of the best-documented UV/blue tuning sites (Rhodopsin site 90), the planthopper blue-shifted UV-opsin paralogs retained the ancestral lysine at this position. Combined, the new findings identify aphid and planthopper UV-opsins as a new valuable data sample for studying adaptive opsin evolution.