Disease Epidemiology in Arthropods Is Altered by the Presence of Nonprotective Symbionts

Abstract

Inherited microbial symbionts can modulate host susceptibility to natural enemy attack. A wider range of symbionts influence host population demography without altering individual susceptibility, and it has been suggested that these may modify host disease risk through altering the rate of exposure to natural enemies. We present the first test of this thesis, specifically testing whether male-killing symbionts alter the epidemiology of a sexually transmitted infection (STI) carried by its host. STIs are typically expected to show female-biased epidemics, and we first present a simple model which indicates that male-biased STI epidemics may occur where symbionts create female-biased population sex ratios. We then examined the dynamics of a STI in the ladybird beetle Adalia bipunctata, which is also host to a male-killing bacterium. We present evidence that male-biased epidemics of the STI are observed in natural populations when the male-killer is common. Laboratory experiments did not support a role for differential susceptibility of male and female hosts to the STI, nor a protective role for the symbiont, in creating this bias. We conclude that the range of symbionts likely to alter parasite epidemiology will be much wider than previously envisaged, because it will additionally include those that impact host demography alone.

Assessing the impact of male-killing bacteria on the spread of a sexually transmitted infection

“…Where mating occurred, the recipient females were then maintained at 22 C to ensure consistency of treatment (mite latent period is thermally sensitive). The number of larval mites on the female was recorded 24 h later, and we monitored the development of these infections by scoring mite infection again after 14 days, the time at which onward infection becomes possible (Ryder et al, 2014). The experiment was performed over three blocks with 10 frequent-opportunity and 10 standard-opportunity mating male ladybirds per block, for a total of 30 males per treatment.…”

“…Approximately 10% of beetles emerge from overwintering carrying the mite infection, and this infection spreads through the cohort during the spring reproductive period, during which females mate approximately once every 2 days. A previous model investigated the impact of population sex ratio bias on STI dynamics in this system (Ryder et al, 2014). The model comprised a series of coupled differential equations describing the within-generation dynamics of uninfected (U), exposed but uninfectious (E) and infectious (I) individuals in male (M) and female (F) hosts (six types of individual).…”

“…Here, male-biased epidemics of the STI are observed, in which male beetles become infected with mites on average 10 days before female beetles. In contrast, in areas where the Spiroplasma is rare, epidemic spread of the STI occurs at equivalent rates in male and female hosts (Ryder et al, 2014).…”

“…Recent work has established male-biased patterns of STI spread in natural populations of the two-spot ladybird, Adalia bipunctata (Ryder et al, 2014). This species is host to the mite Coccipolipus hippodamiae, which transfers between host individuals while they copulate, and thus is an STI.…”

“…An infected host will produce a limited number of larval mites each day (one mature adult mite lays one to three eggs per day; wild female ladybirds carry one to six mature female mites). While larval mite supply is sufficient to create very high per copulation transmission efficiency at low mating rates (Hurst et al, 1995;Ryder et al, 2014), a rapid remating rate may diminish the 'pool' of larval mites waiting to transfer, impacting on the probability of mite acquisition following copulation. This would then buffer the population against increased transmission opportunity associated with a biased sex ratio.…”