Fitness costs of animal medication: antiparasitic plant chemicals reduce fitness of monarch butterfly hosts

Abstract

The emerging field of ecological immunology demonstrates that allocation by hosts to immune defence against parasites is constrained by the costs of those defences. However, the costs of non-immunological defences, which are important alternatives to canonical immune systems, are less well characterized. Estimating such costs is essential for our understanding of the ecology and evolution of alternative host defence strategies. Many animals have evolved medication behaviours, whereby they use antiparasitic compounds from their environment to protect themselves or their kin from parasitism. Documenting the costs of medication behaviours is complicated by natural variation in the medicinal components of diets and their covariance with other dietary components, such as macronutrients. In the current study, we explore the costs of the usage of antiparasitic compounds in monarch butterflies (Danaus plexippus), using natural variation in concentrations of antiparasitic compounds among plants. Upon infection by their specialist protozoan parasite Ophryocystis elektroscirrha, monarch butterflies can selectively oviposit on milkweed with high foliar concentrations of cardenolides, secondary chemicals that reduce parasite growth. Here, we show that these antiparasitic cardenolides can also impose significant costs on both uninfected and infected butterflies. Among eight milkweed species that vary substantially in their foliar cardenolide concentration and composition, we observed the opposing effects of cardenolides on monarch fitness traits. While high foliar cardenolide concentrations increased the tolerance of monarch butterflies to infection, they reduced the survival rate of caterpillars to adulthood. Additionally, although non-polar cardenolide compounds decreased the spore load of infected butterflies, they also reduced the life span of uninfected butterflies, resulting in a hump-shaped curve between cardenolide non-polarity and the life span of infected butterflies. Overall, our results suggest that the use of antiparasitic compounds carries substantial costs, which could constrain host investment in medication behaviours.

Host Diet Affects the Morphology of Monarch Butterfly Parasites

“…While the exact mechanism by which cardenolides reduce parasite growth and virulence remains unclear, the current study provides a likely explanation for the observed increases in parasite tolerance of monarchs feeding on high-cardenolide milkweed (Sternberg et al, 2012;Tao et al, 2015Tao et al, , 2016. Butterflies fed on high-cardenolide milkweed have higher tolerance, meaning they suffer less fitness loss with increasing parasite spore loads than do monarchs reared on low-cardenolide milkweed.…”

“…Previous studies have shown that infected monarchs reared on milkweeds with high cardenolide concentrations exhibit reduced parasite loads and increased tolerance to parasites (de Roode et al, 2008a(de Roode et al, , 2011aLef`evre et al, 2010;Sternberg et al, 2012;Gowler et al, 2015;Tao et al, 2015Tao et al, , 2016. Cardenolides may cause these reductions in parasite loads by increasing host immunity to the parasite, as has been seen in other systems (Lee et al, 2008;Povey et al, 2009;Simpson et al, 2015), or by direct inhibition of parasites (Cory and Hoover, 2006).…”

“…Many previous studies have documented the antimicrobial, antiviral, anti-parasitic, and anti-cancer qualities of plant secondary chemicals (Ohigashi et al, 1992;Murakami et al, 1994Murakami et al, , 1996Billing and Sherman, 1998;Sherman and Billing, 1999). In the monarch-parasite system, infected monarch butterflies have shown decreases in parasite loads and increases in tolerance to O. elektroscirrha when reared on milkweeds with higher cardenolide concentrations (de Roode et al, 2008a(de Roode et al, , 2011bSternberg et al, 2012;Gowler et al, 2015;Tao et al, 2015Tao et al, , 2016. Although the medicinal qualities of numerous plant chemicals are clear (Hunter, 2016), their direct effects on parasite morphology, as well as any related effects on pathogenicity and transmission, are unknown (Okagaki et al, 2010;Zaragoza et al, 2010).…”

Mycorrhizae Alter Toxin Sequestration and Performance of Two Specialist Herbivores

“…Although caterpillars were never food limited in our study, AMF-mediated declines in plant biomass may have reduced caterpillar survival by decreasing the availability of young leaves because monarch caterpillars prefer younger leaves (Bingham and Agrawal, 2010). AMFmediated increases in foliar cardenolide concentrations did not correlate with declines in caterpillar survival in this study, although high cardenolide concentrations often reduce monarch caterpillar performance and survival (Zalucki et al, 2001a;Agrawal, 2005;Rasmann et al, 2009;Tao et al, 2016b).…”

“…Monarch caterpillars, in contrast, have NA + /K + -ATPases that are insensitive to cardenolides (Dobler et al, 2012;Petschenka and Agrawal, 2015). Despite being able to tolerate cardenolides, both oleander aphids and monarch caterpillars exhibit reduced performance on host plants with high concentrations of cardenolides (Zalucki et al, 2001a;Agrawal, 2004Agrawal, , 2005Rasmann et al, 2009;de Roode et al, 2011;Colvin et al, 2013;Tao et al, 2016b;Birnbaum et al, 2017). Furthermore, both oleander aphids and monarch caterpillars sequester cardenolides (Rothschild et al, 1970;Malcolm and Brower, 1989;Malcolm, 1990;Züst and Agrawal, 2016b), providing an effective defense against aphid predators (Pasteels, 1978;Malcolm, 1989Malcolm, , 1992Pappas et al, 2007;Mooney et al, 2008) and monarch predators and parasites (Brower et al, 1968;Reichstein et al, 1968;Brower and Moffitt, 1974;Sternberg et al, 2012).…”