Strength in numbers: high parasite burdens increase transmission of a protozoan parasite of monarch butterflies (Danaus plexippus)
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Parasites often produce large numbers of offspring within their hosts. High parasite burdens are thought to be important for parasite transmission, but can also lower host fitness. We studied the protozoan Ophryocystis elektroscirrha, a common parasite of monarch butterflies (Danaus plexippus), to quantify the benefits of high parasite burdens for parasite transmission. This parasite is transmitted vertically when females scatter spores onto eggs and host plant leaves during oviposition; spores can also be transmitted between mating adults. Monarch larvae were experimentally infected and emerging adult females were mated and monitored in individual outdoor field cages. We provided females with fresh host plant material daily and quantified their lifespan and lifetime fecundity. Parasite transmission was measured by counting the numbers of parasite spores transferred to eggs and host plant leaves. We also quantified spores transferred from infected females to their mating partners. Infected monarchs had shorter lifespans and lower lifetime fecundity than uninfected monarchs. Among infected females, those with higher parasite loads transmitted more parasite spores to their eggs and to host plant leaves. There was also a trend for females with greater parasite loads to transmit more spores to their mating partners. These results demonstrate that high parasite loads on infected butterflies confer a strong fitness advantage to the parasite by increasing between-host transmission.
KeywordsPathogen Virulence Evolution Trade-off Ophryocystis elektroscirrha
We thank B. Ledbetter, C. Norman and A. Pedersen for help with the experiments, A. Tull and the UGA Plant Biology greenhouse staff for access to field plots and greenhouse space, and two anonymous referees for helpful comments. J. C. de Roode was supported by a Netherlands Organization for Scientific Research (NWO) TALENT fellowship, a Marie Curie Outgoing International Fellowship and Emory University. S. Altizer was supported by the University of Georgia and NSF DEB-0643831. The experiments comply with current US laws.
- Altizer SM, Oberhauser KS, Geurts KA (2004) Transmission of the protozoan parasite, Ophryocystis elektroscirrha, in monarch butterfly populations: implications for prevalence and population-level impacts. In: Oberhauser KS, Solensky M (eds) The monarch butterfly: biology and conservation. Cornell University Press, Ithaca, pp 203–218Google Scholar
- Anderson RM, May RM (1992) Infectious diseases of humans—dynamics and control. Oxford University Press, OxfordGoogle Scholar
- Brower LP (1995) Understanding and misunderstanding the migration of the monarch butterfly (Nymphalidae) in North America: 1857–1995. J Lepidopt Soc 49:304–385Google Scholar
- Ebert D (1999) The evolution and expression of parasite virulence. In: Stearns SC (ed) Evolution in health and disease. Oxford University Press, Oxford, pp 161–172Google Scholar
- Leong KLH, Yoshimura MA, Kaya HK (1997b) Occurrence of a neogregarine protozoan, Ophryocystis elektroscirrha McLaughlin and Myers, in populations of monarch and queen butterflies. Pan-Pac Entomol 73:49–51Google Scholar
- McLaughlin RE, Myers J (1970) Ophryocystis elektroscirrha sp. n., a neogregarine pathogen of monarch butterfly Danaus plexippus (L.) and the Florida queen butterfly D. gilippus berenice Cramer. J Protozool 17:300–305Google Scholar
- Prysby MD, Oberhauser K (2004) Temporal and geographic variation in monarch densities: citizen scientists document monarch population patterns. In: Oberhauser K, Solensky M (eds) The monarch butterfly: biology and conservation. Cornell University Press, IthacaGoogle Scholar
- Van Hook T (1993) Non-random mating in monarch butterflies overwintering in Mexico. In: Zalucki MP (ed) Biology and conservation of the monarch butterfly. Natural History Museum of Los Angeles County, Los Angeles, pp 49–60Google Scholar
- Vickerman D, Michels A, Burrowes PA (1999) Levels of infection of migrating monarch monarch butterflies, Danaus plexippus (Lepidoptera: Nymphalidae) by the parasite Ophryocystis elektroscirrha (Neogregarinidae: Ophryocystidae), and evidence of a new mode of spore transmission between adults. J Kans Entomol Soc 72:124–128Google Scholar