Physiological and Environmental Factors Affecting the Composition of the Ejaculate in Mosquitoes and Other Insects

insects Review Physiological and Environmental Factors Affecting the Composition of the Ejaculate in Mosquitoes and Other Insects Megan E. Meuti * and Sarah M. Short Department of Entomology, The Ohio State University, 2001 Fyffe Rd., Room 232 Howlett Hall, Columbus, OH 43210, USA; [email protected] * Correspondence: [email protected] Received: 23 January 2019; Accepted: 8 March 2019; Published: 15 March 2019 Abstract: In addition to transferring sperm, male mosquitoes deliver several proteins, hormones and other factors to females in their seminal fluid that inhibit remating, alter host-seeking behaviors and stimulate oviposition. Recently, bioinformatics, transcriptomics and proteomics have been used to characterize the genes transcribed in male reproductive tissues and the individual proteins that are delivered to females. Thanks to these foundational studies, we now understand the complexity of the ejaculate in several mosquito species. Building on this work, researchers have begun to identify the functions of various proteins and hormones in the male ejaculate, and how they mediate their effects on female mosquitoes. Here, we present an overview of these studies, followed by a discussion of an under-studied aspect of male reproductive physiology: the effects of biotic and abiotic factors on the composition of the ejaculate. We argue that future research in this area would improve our understanding of male reproductive biology from a physiological and ecological perspective, and that researchers may be able to leverage this information to study key components of the ejaculate. Furthermore, this work has the potential to improve mosquito control by allowing us to account for relevant factors when implementing vector control strategies involving male reproductive biology. Keywords: mosquito; male accessory glands; accessory gland proteins; seminal fluid; sperm; body size; larval crowding; nutrition; temperature; seasonal cues 1. Introduction Mosquitoes are by far the deadliest animals known to man, transmitting pathogens like the malaria parasite, and viruses such as yellow fever, dengue, chikungunya, Zika and West Nile which collectively claim hundreds of thousands of human lives each year [1]. Furthermore, mosquitoes threaten our pets and livestock by transmitting pathogens such as canine heartworm and the Eastern equine encephalitis virus [2,3]. Vertebrates become infected with these pathogens when an infective female mosquito takes a blood meal and transmits them from her salivary glands into the vertebrate blood. Although male mosquitoes never blood feed, and therefore do not transmit pathogens, they play a critical role in maintaining the mosquito population. Reducing the mosquito population is a primary line of defense against all of these diseases, and multiple proposed vector control methods rely on releasing sterile or genetically modified males that produce no offspring when mated with wild females [4–6]. It is also possible to genetically engineer mosquitoes to be more resistant to pathogens, and to propagate these traits using reproductive gene drives [7]. Due to this promising role in vector control, male mosquito reproductive biology and the ejaculate they transfer to female mosquitoes has been a subject of growing interest (see review by [8]). We have long known that in addition to transferring sperm, male mosquitoes and other animals (arthropods, reptiles/amphibians, birds and mammals) transfer a variety of factors in their seminal Insects 2019, 10, 74; doi:10.3390/insects10030074 www.mdpi.com/journal/insects Insects 2019, 10, x FOR PEER REVIEW 2 of 18 Insects 2019, 10, 74 2 of 18 We have long known that in addition to transferring sperm, male mosquitoes and other animals (arthropods, reptiles/amphibians, birds and mammals) transfer a variety of factors in their seminal fluid thatfluid notthatonly not only activate activate sperm sperm and and enhance enhance its its motilitymotility and storage, storage, but but also also have have profound profound influencesinfluences on female on female behavior, behavior, reproductive reproductive physiology physiology andand fecundity. Proteins Proteins in inthe the seminal seminal fluid fluid are primarilyare primarily produced produced in the in the male male accessory accessory glands glands andand thethe seminal vesicles, vesicles, ejaculatory ejaculatory duct duct and and bulb (Figurebulb (Figure1). Possibly, 1). Possibly the,testes the testes produce produce seminal seminal fluid fluid proteins proteins asas well. Collective Collectivelyly these these seminal seminal fluid proteinsfluid proteins (SFPs) (SFPs) combined combined with with hormones, hormones, carbohydrates, carbohydrates, salts, and and lipids lipids make make up upthe theseminal seminal fluid [9fluid], and [9], the and seminal the seminal fluid fluid along along with with sperm sperm compose compose the male male ejaculate ejaculate (as (as reviewed reviewed in [10 in– [15]10).–15 ]). Decades of work primarily in the fruit fly, Drosophila melanogaster, have elucidated the specific effects Decades of work primarily in the fruit fly, Drosophila melanogaster, have elucidated the specific effects of multiple components of the ejaculate, the molecular interactions among these components, their of multiple components of the ejaculate, the molecular interactions among these components, their mode of action in the female, and the evolutionary dynamics of genes that code for SFPs (reviewed modeby of [10,11] action). in This the seminal female, work and (pun the intended) evolutionary in a model dynamics organism of genes has provided that code a critical for SFPs foundation (reviewed by [10,allowing11]). This further seminal exploration work (pun of seminal intended) fluid in biology a model in other organism organisms. has provided a critical foundation allowing further exploration of seminal fluid biology in other organisms. Figure 1. Morphology of the male reproductive tract in (A) Anopheles gambiae,(B) Culex pipiens and Figure 1. Morphology of the male reproductive tract in (A) Anopheles gambiae, (B) Culex pipiens and (C) Aedes aegypti. MAG = male accessory gland, SV = seminal vesicle, ED = ejaculatory duct. (C) Aedes aegypti. MAG = male accessory gland, SV = seminal vesicle, ED = ejaculatory duct. BuildingBuilding on this on substantialthis substantial body body of of work, work, we we are are nownow beginningbeginning to to understand understand the the functional functional role ofrole several of several components components of the of the seminal seminal fluid fluid in in mosquitoes mosquitoes and other other insects, insects, including including how how they they mediatemediate their effectstheir effects on female on female behavior, behavior, physiology physiology and and fecundity. fecundity. However, However, there there is stillis still much much work to be donework hereto be due done in here large due part in to large the complexitypart to the complexity of seminal of fluids. seminal To fluids. date, mostTo date, of the most research of the has mainlyresearch focused has on mainly characterizing focused on the characterizing proteins in the the proteins ejaculate, in the which ejaculate, are highly which diverse.are highly For diverse. example, a combinationFor example, of bioinformatic a combination of and bioinformatic microarray and analyses microarray have analyses identified have 121 identified transcripts 121 transcripts produced in the maleproduced accessory in the glands male accessory in the malaria glands mosquito,in the malariaAnopheles mosquito, gambiae Anopheles[12 ,gambiae16,17], and[12,16,17] a recent, and study a recent study demonstrates that males of the yellow fever mosquito, Aedes aegypti, transfer 870 sperm demonstrates that males of the yellow fever mosquito, Aedes aegypti, transfer 870 sperm proteins proteins and 280 SFPs to females during mating [18]. Another growing field of research has focused and 280 SFPs to females during mating [18]. Another growing field of research has focused on the on the evolutionary biology of SFPs (see reviews by [14,19,20]). This work has demonstrated that evolutionaryalthough biology the classes of SFPs of proteins (see reviews found by in [the14, 19seminal,20]). Thisfluids work are well has- demonstratedconserved across that mosquitoes although the classesand of proteinsother insect found species, in the there seminal is a high fluids degree are of well-conserved variation in the number across mosquitoesand type of the and individual other insect species,components there is a highwithin degree these ofclasses variation even inbetween the number closely and-related type species, of the individual such as Ae. components aegypti and Ae. within these classesalbopictus even [18,21] between. Among closely-related anophelines species,there is evidence such as Ae. of at aegypti least oneand recentAe. albopictus expansion[18 of,21 a]. male Among anophelinesaccessory there gland is evidencespecific gene of atfamily least [22] one. Additionally, recent expansion Izquierdo of a maleet al. [23] accessory showed gland that some specific male gene familyreproductive [22]. Additionally, transcripts Izquierdo have consistent et al. [23 patterns] showed of thatgene someexpression male across reproductive the Anopheles transcripts gambiae have consistentspecies patterns complex, of but gene othe expressionrs have lineage across-specific the Anopheles expression gambiae profiles.species This suggests complex, that genes but others coding have for components of the ejaculate

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