Abstract
Adaptive traits that enable organisms to conquer novel niches and experience subsequent diversification are ecologically and evolutionarily important. The larvae of Pieris butterflies express nitrile-specifier proteins (NSPs), a key innovation for overcoming the glucosinolate (GLS)-myrosinase-based defence system of their Brassicales host plants. Nitrile-specifier proteins are a member of the NSP-like gene family, which includes the major allergen (MA) protein, a paralog of NSP with a GLS-disarming function, and a single domain major allergen (SDMA) protein, whose function is unknown. The arms-race between GLS-based defences and the NSP-like gene family is suggested to mediate diversification in both Pierid butterflies and Brassicales plants. Here, we tested whether the expected strong selection on NSP-like gene family correlates with shifts in host plant spectra among Pierid butterflies. We combined feeding experiments using 25 Brassicaceae plants and five Pieris species with larval transcriptome data to investigate the patterns of selection acting on NSP-like gene family members. Although we observed significantly elevated nonsynonymous to synonymous substitution rate ratios in NSPs on branches associated with changes in patterns of host plant usage, no such pattern was observed in MAs or SDMAs. Furthermore, we found evidence for positive selection of NSP at a phylogenetic branch which reflects different host plant spectra. Our data indicate that the NSP-related gene members have evolved differently: NSPs have accumulated more amino acid changes in response to shifting preferences for host plants, whereas MAs and SDMAs appear to be more conserved. Further detailed functional assays of these genes would provide important insights to understand their role in the chemical arms-race between Pieris butterflies and their Brassicales host plants.
Highlights
Key innovations that enable organisms to acquire novel niches and experience subsequent radiation are ecologically and evolutionarily important (Bond & Opell, 1988; Hunter, 1998)
single domain major allergen (SDMA) is generally expressed in the guts of Lepidopteran larvae, nitrile‐specifier proteins (NSPs) and major allergen (MA) are only found in Pierid but‐ terflies feeding on Brassicales (Fischer et al, 2008; Randall, Perera, London, & Mueller, 2013)
Focusing on five Japanese Pieris butterflies, we tested host plant spec‐ tra and investigated signatures of selection on NSP‐like genes, which are a key innovation of these butterflies to overcome the GLS defence system of their Brassicales host plants (Edger et al, 2015; Wheat et al, 2007)
Summary
Key innovations that enable organisms to acquire novel niches and experience subsequent radiation are ecologically and evolutionarily important (Bond & Opell, 1988; Hunter, 1998). SDMA is generally expressed in the guts of Lepidopteran larvae, NSP and MA are only found in Pierid but‐ terflies feeding on Brassicales (Fischer et al, 2008; Randall, Perera, London, & Mueller, 2013) These findings suggest that in Pieris, MAs, like NSPs, have a function related to disarming GLSs. The ability of MA to redirect GLS hydrolysis was recently documented in one Brassicales‐feeding Pierid, Anthocharis cardamines, which seems to have MA genes only, that is, it lacks NSP (Edger et al, 2015; In this study, “NSP” was used to name NSP‐like gene family members, in‐ cluding MA). The obtained results provide important insights into the evolution of adaptive key innovations in Pieris butterflies
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