Gimme shelter – the relative sensitivity of parasitic nematodes with direct and indirect life cycles to climate change

Abstract

Climate change is expected to alter the dynamics of host-parasite systems globally. One key element in developing predictive models for these impacts is the life cycle of the parasite. It is, for example, commonly assumed that parasites with an indirect life cycle would be more sensitive to changing environmental conditions than parasites with a direct life cycle due to the greater chance that at least one of their obligate host species will go extinct. Here, we challenge this notion by contrasting parasitic nematodes with a direct life cycle against those with an indirect life cycle. Specifically, we suggest that behavioral thermoregulation by the intermediate host may buffer the larvae of indirectly transmitted parasites against temperature extremes, and hence climate warming. We term this the 'shelter effect'. Formalizing each life cycle in a comprehensive model reveals a fitness advantage for the direct life cycle over the indirect life cycle at low temperatures, but the shelter effect reverses this advantage at high temperatures. When examined for seasonal environments, the models suggest that climate warming may in some regions create a temporal niche in mid-summer that excludes parasites with a direct life cycle, but allows parasites with an indirect life cycle to persist. These patterns are amplified if parasite larvae are able to manipulate their intermediate host to increase ingestion probability by definite hosts. Furthermore, our results suggest that exploiting the benefits of host sheltering may have aided the evolution of indirect life cycles. Our modeling framework utilizes the Metabolic Theory of Ecology to synthesize the complexities of host behavioral thermoregulation and its impacts on various temperature-dependent parasite life history components in a single measure of fitness, R0 . It allows quantitative predictions of climate change impacts, and is easily generalized to many host-parasite systems.

Invasion, establishment, and range expansion of two parasitic nematodes in the Canadian Arctic

“…In contrast to assertions that responses for host‐pathogen assemblages to climate warming will involve shifts in distribution we suggest, based on an unequivocal and ongoing expansion event onto Victoria Island, that the range of interactions among hosts, pathogens and climate will be more nuanced, involving multiple mechanisms, including broadened ranges overall for some assemblages (also see Molnar et al 2013 Brooks & Hoberg, ; Burek et al ., ; Molnár et al . ). This may be particularly true for parasites like the protostrongylids that have life history strategies (i.e., sheltered in gastropods) that allow them to cope with extremes in temperatures (Molnár et al ., 2013a).…”

Skewed temperature dependence affects range and abundance in a warming world

“…We refer to this relation as coldskewed because the distribution's heavy tail corresponds to cold temperatures (figure 1b). By contrast, environmentally transmitted nematode parasites can exhibit a warm-skewed population growth curve, because the mortality of free-living stages is directly affected by temperature, but reproductionwhen occurring within an endotherm definitive host-is temperature-independent [13] (figures 1c and 2b; see also [14]). Intermediate cases also exist (e.g.…”

Factors influencing mortality of Lesser Scaup (Aythya affinis) ducklings during a West Nile virus outbreak

“…Seasonal patterns in disease exposure may also be an important factor affecting offspring survival in other temperate-breeding organisms. Parasitic nematodes, for example, can cause substantial mortality of wildlifethey also develop more quickly at higher temperatures and infect intermediate hosts that increase in abundance during the breeding season (Kutz et al 2001;Molnár et al 2013).…”