Constraints on the reproductive value of vertical transmission for a microsporidian parasite and its female‐killing behaviour

Abstract

Summary 1. Several species of microsporidian parasites use a mixture of vertical and horizontal transmission among their respective mosquito host species. These relationships vary in how hosts are exploited for either vertical or horizontal transmission. An important factor is that only females can provide vertical transmission. Two types of relationship have particularly been contrasted; those where vertically infected larvae of both sexes are killed late in their development and contribute towards the parasite's horizontal transmission, and those where only male larvae are killed while females experience benign infections, become adults, and contribute towards the parasite's vertical transmission success. The selective killing of males in these latter relationships leads to female‐biased adult sex ratios. These differences among relationships have been suggested to depend on the environmental conditions they experience and on the relative efficiency of vertical or horizontal transmission. 2. The transmission behaviour of the microsporidian parasite Edhazardia aedis (Becnel, Fukuda & Sprague) following vertical transmission was studied as a function of larval food availability to its host, the mosquito Aedes aegypti (L.). The number of vertically infected mosquitoes dying before reaching adulthood increased as larval food availability became less. However, proportionately more females died as food availability decreased and adult mosquito populations became increasingly male‐biased. 3. The fate of vertically infected mosquitoes was closely related to their larval growth rate. As food availability decreased and larval growth rates slowed, the parasite's infection had more time to produce its spores and induce the host's mortality before emergence. This disproportionately affected female mosquitoes as they pupate later than males, especially as larval growth rates slow. As late ages at pupation are associated with smaller adult size (≈ lower fecundity), the potential vertical transmission offered by slowly growing female larvae is limited and more success may be gained by exploiting them for horizontal transmission. 4. Our results indicate that the relative reproductive value of vertical or horizontal transmission altered with an ecological parameter (larval food availability). Constraints in the life‐history traits of each organism helped to explain why the observed sex ratio was biased towards males rather than females.