Biological rhythms are found across life and enable organisms to coordinate with the cyclic changes of the environment (be it daily changes in light, humidity, abundance of food, predator/prey interactions). How biological rhythms influence infection is often overlooked but timing can determine mortality rate, severity of infection, and transmission (see reviews here and here).
For malaria, the biological rhythms of the mammalian host, the mosquito vector and the parasite interact. It is important to understand these interactions so that we may predict the outcome for disease transmission when the rhythms of one or all parties change. For example, some mosquito populations are shifting the time of day they forage for blood to evade insecticide treated bed nets.
Malaria-transmitting mosquitoes are primarily night biters, and so, many of their biologically processes are timed to anticipate this behaviour (e.g. olfactory senses are more sensitive at night compared to daytime). Blood feeding is a metabolically costly and physically intense event for mosquitoes (imagine eating an entire roast turkey, now imagine doing so at 4am) so altering feeding timing may have consequences for mosquito life history, which in turn, could affect the transmission prospects of malaria parasites.
Our recently published research article is composed of three independent experiments that test the impact of morning versus evening blood feeding for mosquito survival and reproductive metrics.
We focus on whether 1) host blood quality (anaemic or not), 2) host circadium rhythms or 3) malaria infection interact with the timing of blood feeding to alter the lifespan and reproductive output of mosquitos. Further, we also examine the impact of time of day of blood feeding for the intensity and prevalence of malaria parasites in mosquitos.
A labor-intensive project
In practice, this meant working with 2400 mosquitoes, 1200 of which were individually housed, each of which need daily mortality/egg lay checks as well as making sure their sugar source is plentiful enough to keep them alive but not so plentiful that it drips and the mosquitoes kill themselves on a sticky trap. An oviposition habitat needed to be provided, nice enough to encourage egg lay but not so big that the female drowns herself. Blood meals had to occur both early in the morning and late at night which required monitoring 24 anaesthetized mice at once and then transferring every fed mosquito to their new home, gently enough so that they don’t explode and die. Many students were involved in the success of these logistics.
Consequences of changing mealtime
We found that the timing of a blood meal has no impact on the lifespan of mosquitos but does have several effects on reproductive metrics, including the likelihood to lay eggs and the timing of oviposition. Mosquitoes that fed in the morning are more likely to lay eggs, lay sooner and have larger clutch sizes.
Further, in keeping with other studies, malaria (Plasmodium berghei) infection reduces mosquito lifespan by approximately three days, but this is not influenced by the time of day that the mosquito takes a blood meal. These results suggest that there is previously unknown flexibility in mosquito physiology that allows them to cope with changes in timing in events such as blood-feeding.
That the timing of a P. berghei infected blood meal does not alter transmission prospects suggests that mosquito rhythms are not important. However, we suspect this is an oversimplification: P. berghei is an asynchronously (not synchronised) developing parasite in the host, which may mean it is similarly unaffected by vector rhythms. In contrast, recent findings show that transmission of the synchronous parasite P. chabaudi is shaped by a combination of parasite timing and mosquito timing.
Overall, we find that time-of-day of blood feeding has minor effects on mosquitoes. Feeding in the morning increases the reproductive output of females, but doesn’t seem to directly impact malaria transmission. To what extent this is because our “mosquito condos” provided mosquitoes with a lot of everything they needed, compensating for any costs of daytime feeding, is yet to be determined. However, if our results hold for wild mosquitoes that have changed their biting time, and human parasites, then malaria transmission may be able to increase due to increases in mosquito populations.