CCAP and FMRFamide-like peptides accelerate the contraction rate of the antennal accessory pulsatile organs (auxiliary hearts) of mosquitoes

Abstract

Insects rely on specialized accessory pulsatile organs (APOs), also known as auxiliary hearts, to propel hemolymph into their antennae. In most insects, this is accomplished via the pulsations of a pair of ampulla located in the head, each of which propels hemolymph across an antenna via an antennal vessel. Once at the distal end of the appendage, hemolymph returns to the head via the antennal hemocoel. Although the structure of the antennal hearts has been elucidated in various insect orders, their hormonal modulation has only been studied in cockroaches and other hemimetabolous insects within the superorder Polyneoptera, where proctolin and FMRFamide-like peptides accelerate the contraction rate of these auxiliary hearts. Here, we assessed the hormonal modulation of the antennal APOs of mosquitoes, a group of holometabolous (Endopterygota) insects within the order Diptera. We show that crustacean cardioactive peptide (CCAP), FMRFamide and SALDKNFMRFamide increase the contraction rate of the antennal APOs and the heart of Anopheles gambiae. Both antennal hearts are synchronously responsive to these neuropeptides, but their contractions are asynchronous with the contraction of the heart. Furthermore, we show that these neuropeptides increase the velocity and maximum acceleration of hemolymph within the antennal space, suggesting that each contraction is also more forceful. To our knowledge, this is the first report demonstrating that hormones of a holometabolous insect modulate the contraction dynamics of an auxiliary heart, and the first report that shows that the hormones of any insect accelerate the velocity of hemolymph in the antennal space.

Hemolymph circulation in insect flight appendages: physiology of the wing heart and circulatory flow in the wings of the mosquito,Anopheles gambiae

“…This independence is reminiscent of the independence between the dorsal vessel and another type of accessory pulsatile organ: the antennal heart. In both mosquitoes and cockroaches, there is no correlation between the contraction rate of the antennal hearts and the dorsal vessel, but different from what we observed for the wing heart, the antennal hearts contract at a significantly slower rate than the dorsal vessel (Hertel et al, 1985;Boppana and Hillyer, 2014;Suggs et al, 2016). Furthermore, some cardioacceleratory peptides, such as CCAP, FMRFamides and proctolin, are known to modulate the contraction dynamics of both the dorsal vessel and the antennal hearts of insects (Cuthbert and Evans, 1989;Predel et al, 2004;Ejaz and Lange, 2008;Hertel et al, 2012;Estevez-Lao et al, 2013;Suggs et al, 2016).…”

“…Similarly, the maximum acceleration of hemolymph is nearly 14 times greater when it exits the wing than when it enters it. For insects, data on hemolymph flow dynamics are sparse, but the data in the present study follow a comparable pattern to what we have observed for the antennal space of mosquitoes: velocity and maximum acceleration are highest near the contractile pump (Boppana and Hillyer, 2014;Suggs et al, 2016). In the case of the antennal heart, hemolymph velocity is fastest near the pump because the diameter of the antennal vessel that extends from the pump is narrower than the diameter of the antennal hemocoel into which it empties.…”

“…By that logic, we hypothesize that the combined cross-sectional area of the afferent wing veins is larger than the combined cross-sectional area of the efferent wing veins. Even though the relative patterns of velocity and maximum acceleration are similar between the wing heart and the antennal hearts of mosquitoes, a significant difference between these two pulsatile organs pertains to the mechanics of flow: the wing heart aspirates hemolymph out of the appendages whereas the antennal hearts propel hemolymph into the appendages (Boppana and Hillyer, 2014;Suggs et al, 2016).…”

Crustacean cardioactive peptides: Expression, localization, structure, and a possible involvement in regulation of egg-laying in the cuttlefish Sepia officinalis

“…Still in L. migratoria, CCAP-like immunostained cells were discovered in the fat body associated with the oviducts that represents a potential source of CCAP, along the transverse nerve and perivisceral organs. In the mosquito A. gambiae, CCAP increased the contraction rate of the auxiliary hearts, the organ that controls hemolymph circulation in the antennae (Suggs et al, 2016). In S. officinalis CCAPs increased the vena cava tonus in a dose-dependent manner; this demonstrates their involvement in the regulation of hemolymph circulation (data not shown).…”

Distribution of FMRFamide-related peptides and co-localization with glutamate in Cupiennius salei, an invertebrate model system

“…One example is the excitatory action of FaRPs in chromatophore neuromuscular junctions of the cuttlefish Sepia officinalis (Loi and Tublitz 2000, see discussion). In auxiliary hearts of mosquitoes that propel hemolymph into the antennae of the insects FaRPs have accelerating effects (Suggs et al, 2016). Although the presence of FaRPs has been described in the visual system and along mechanosensory neurons of C. salei, Schmid 1999, Fabian-Fine et al, 2017) the distribution of these neuropeptides throughout the rest of the spider nervous system has not been described in detail.…”