Abstract
Lepidoptera is amongst one of the four most speciose insect orders and ecologically very successful because of their ability to fly. Insect flight is always aerobic and exacts a high metabolic demand on the animal. A family of structurally related neuropeptides, generically referred to as adipokinetic hormones (AKHs), play a key role in triggering the release of readily utilizable fuel metabolites into the hemolymph from the storage forms in the fat body. We used mass spectrometry to elucidate AKH sequences from 34 species of Lepidoptera and searched the literature and publicly available databases to compile (in a phylogenetic context) a comprehensive list of all Lepidoptera sequences published/predicted from a total of 76 species. We then used the resulting set of 15 biochemically characterized AKHs in a physiological assay that measures lipid or carbohydrate mobilization in three different lepidopteran species to learn about the functional cross-activity (receptor-ligand interactions) amongst the different butterfly/moth families. Our results include novel peptide structures, demonstrate structural diversity, phylogenetic trends in peptide distribution and order-specificity of Lepidoptera AKHs. There is almost an equal occurrence of octa-, nona-, and decapeptides, with an unparalleled emphasis on nonapeptides than in any insect order. Primitive species make Peram-CAH-II, an octapeptide found also in other orders; the lepidopteran signature peptide is Manse-AKH. Not all of the 15 tested AKHs are active in Pieris brassicae; this provides insight into structure-activity specificity and could be useful for further investigations into possible biorational insecticide development.
Highlights
Butterflies are esthetically beautiful and, collected by many laymen enthusiasts but are displayed for the general public in “butterfly houses.” The negative impact of certain Lepidoptera are known, e.g., the larvae of the fall and African armyworms (Spodoptera frugiperda and Spodoptera exempta; superfamily: Noctuoidea) damage crops that are the main staple food sources of people (Baudron et al, 2019); the Indian meal moth larvae (Plodia interpunctella; superfamily: Pyraloidea) devour stored food products, and species of the genera Tinea and Tineola feed on woolen textiles (Basuk and Behera, 2018)
Further beneficial traits of Lepidoptera are the following, to name a few that are relevant to South Africa: (i) economically important sericulture with the domesticated Bombyx mori and wild silk production using the African wild silk moth Gonometa postica (Teshome et al, 2014). (ii) biological weed control, e.g., larvae of the cactus moth, Cactoblastis cactorum, control invasive Opuntia species introduced to Australia and South Africa (Anneke and Moran, 1978). (iii) Larvae of various species are sought-after delicacies for human populations in several countries worldwide: the high demand for Mopane worm in southern Africa (Emperor moth Gonimbrasia belina; superfamily: Bombycoidea) drives a lucrative market for women who collect the larvae in a sustainable manner (Sekonya et al, 2020)
Biological assays were performed with a few lepidopteran species to screen for hyperlipemic hypertrehalosemic activity embedded in the tested CC
Summary
Butterflies are esthetically beautiful and, collected by many laymen enthusiasts but are displayed for the general public in “butterfly houses.” The negative impact of certain Lepidoptera are known, e.g., the larvae of the fall and African armyworms (Spodoptera frugiperda and Spodoptera exempta; superfamily: Noctuoidea) damage crops that are the main staple food sources of people (Baudron et al, 2019); the Indian meal moth larvae (Plodia interpunctella; superfamily: Pyraloidea) devour stored food products, and species of the genera Tinea and Tineola (superfamily: Tineoidea) feed on woolen textiles (Basuk and Behera, 2018). In Lepidoptera the first AKH that was completely structurally elucidated came from the CC of the tobacco hornworm moth, M. sexta (Family: Sphingidae) – the nonapeptide is called ManseAKH (pELTFTSSWG amide; Ziegler et al, 1985), and it functions as a true adipokinetic, lipid-mobilizing, hormone in the adult moth and regulates carbohydrate metabolism in the larval stage (Ziegler et al, 1990). A decapeptide that had some adipokinetic and pronounced trehalose-elevating activity in the cornear moth Heliothis (=Helicoverpa) zea (family: Noctuidae) was sequenced from the CC of this species and was, called a hypertrehalosemic hormone (Helze-HrTH, pELTFSSGWGN amide; Jaffe et al, 1988) It has since been found in other noctuids as well (see Table 1).
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