Sexually transmitted diseases of insects: distribution, evolution, ecology and host behaviour

Abstract

Sexually transmitted diseases (STDs) of insects are known from the mites, nematodes, fungi, protists and viruses. In total 73 species of parasite and pathogen from approximately 182 species of host have been reported. Whereas nearly all vertebrate STDs are viruses or bacteria, the majority of insect STDs are multicellular ectoparasites, protistans or fungi. Insect STDs display a range of transmission modes, with 'pure' sexual transmission only described from ectoparasites, all of which are mites, fungi or nematodes, whereas the microparasitic endo-parasites tend to show vertical as well as sexual transmission. The distribution of STDs within taxa of insect hosts appears to be related to the life histories of the hosts. In particular, STDs will not be able to persist if host adult generations do not overlap unless they are also transmitted by some alternative route. This explains the observation that the Coleoptera seem to suffer from more STDs than other insect orders, since they tend to diapause as adults and are therefore more likely to have overlapping generations of adults in temperate regions. STDs of insects are often highly pathogenic, and are frequently responsible for sterilizing their hosts, a feature which is also found in mammalian STDs. This, combined with high prevalences indicates that STDs can be important in the evolution and ecology of their hosts. Although attempts to demonstrate mate choice for uninfected partners have so far failed it is likely that STDs have other effects on host mating behaviour, and there is evidence from a few systems that they might manipulate their hosts to cause them to mate more frequently. STDs may also play a part in sexual conflict, with males in some systems possibly gaining a selective advantage from transmitting certain STDs to females. STDs may well be important factors in host population dynamics, and some have the potential to be useful biological control agents, but empirical studies on these subjects are lacking.

What Use Are Male Hosts? The Dynamics of Maternally Inherited Bacteria Showing Sexual Transmission or Male Killing

“…Indeed, sexually transmitted strains were observed to take over from existing infections following such a coinfection event. The study of aphid secondary symbionts complements previous work describing male-to-female sexual transmission for a variety of viral and microsporidial associates of insects that also showed maternal inheritance (reviewed in Knell and Webberley 2004), records of a low level of paternal transmission for Wolbachia (Hoffmann and Turelli 1988), and a more recent record of sexual transmission of the bacterium Asaia that is maternally inherited in Anopheles mosquitoes (Favia et al 2007). …”

“…Late MK is often caused by vertically transmitted microsporidia, which gain horizontal transmission out of larval male hosts (Hurst 1991;Hurst et al 2003). Given that microsporidia in various hosts are known to be transmitted from male to female during host copulation, as well as vertically (see Knell and Webberley 2004 for a review), one can imagine a similar tension for the case of late MK, where alternative strategies of horizontal transmission from males through host lysis, and horizontal transmission through copulation, exist.…”

Evolutionary bi-stability in pathogen transmission mode

“…Two broad categories of transmission mode are horizontal transmission, in which the pathogen infects another host irrespective of relationship, and vertical transmission, in which the pathogen infects the host's offspring. Many pathogens of humans, animals and plants spread by a combination of horizontal and vertical transmission (Ewald 1987(Ewald , 1994Power 1992;Knell & Webberley 2004;Verdonck et al 2007;Jestoi 2008). For example, the protozoan parasite Ophryocystis elektroscirrha of the monarch butterfly (Danaus plexippus) is transmitted horizontally when adult butterflies ingest spores on host plant leaves, and is transmitted vertically when spores are transmitted to the outside of the eggs (de Roode et al 2008).…”

Measuring the transmission dynamics of a sexually transmitted disease

“…Unlike other types of directly transmitted infectious disease, STDs are not expected to have threshold densities for persistence, they may cause deterministic extinction, and it is thought that they cannot regulate their host's population size alone (6-8). Critically, even though STDs are now known to occur throughout the animal kingdom (16,18), the only experimental assessment of STD transmission dynamics to date was in a plant. That study (19)(20)(21) provided evidence of frequency-dependent transmission of a pollinator-mediated ''STD'' in the plant system (anther-smut fungus on Silene alba), but there have been no experimental tests of whether transmission is frequency-dependent for animal (or human) STDs.…”

“…In many invertebrates, for example, the mating system of the host may show marked density-dependent variation in sexual contact rate (see the supporting information, which is published on the PNAS web site). STDs are known to be widespread in these taxa (16,18), and many are of huge importance in ecological, socioeconomic, and medical terms. Two major arboviruses, for example, are sexually transmitted within their arthropod vectors: dengue in Aedes albopictus mosquitoes (22), and Crimean-Congo hemorrhagic fever virus in Hyalomma truncatum ticks (23).…”