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Published in final edited form as: Trends Parasitol. 2022 Sep 7;38(11):942–949. doi: 10.1016/j.pt.2022.08.012

Cascading impacts of host seasonal adaptation on parasitism

Naima C Starkloff 1,*, David J Civitello 1
PMCID: PMC9588794  NIHMSID: NIHMS1835148  PMID: 36088213

Abstract

The persistence of parasite populations through harsh seasonal bouts is often critical to circannual disease outbreaks. Parasites have a diverse repertoire of phenotypes for persistence, ranging from transitioning to a different life stage better suited to within-host dormancy to utilizing weather-hardy structures external to hosts. While these adaptive traits allow parasite species to survive through harsh seasons, it is often at survival rates that threaten population persistence. We argue that these periods of parasite (and vector) population busts could be ideal targets for disease intervention. As climate change portends abbreviated host dormancy and extended transmission periods in many host-parasite systems, it is essential to identify novel pathways to sure up current disease intervention strategies.

Keywords: aestivation, dormancy, disease intervention, hibernation, host-parasite, seasonality

Consequences of harsh seasonal climates on parasite persistence

Seasonal variability in climate has challenged species to evolve traits to routinely tolerate harsh abiotic conditions. Many seasonal adaptations involve dormancy (see Glossary), for example, hibernation through cold temperatures of winter seasons is often facilitated by a drop in metabolism and heart rate [1–3] and aestivation to avoid desiccation in dry seasons is possible through metabolic suppression and water retention strategies [4,5]. Other seasonal adaptations include migration [6] or resistance (e.g., anti-freeze proteins [7] and phenotypes for insulation [8]). Individuals carrying out seasonal adaptive behaviors endure harsh physiological stress (such as decreased oxygen availability, loss of body mass, and lactic acid buffering), yet the consequences on the parasites that utilize these hosts are not well understood. Harsh abiotic conditions and host physiological stress may have dire consequences for the parasites that depend on dwindling host resources for within-host survival. Similarly, long periods of inactivity and low contact rates can eliminate between-host transmission opportunities.

Persistence of parasites through harsh seasonal bouts is critical to circannual disease outcomes, yet parasite survival is often limited by the environmental durability of hosts. For example, the fungus Wheat Stripe Rust (Puccinia striiformus), which infects several winter wheat variants (Triticeae species), is less likely to survive overwintering in cultivars with weaker winter hardiness [9]. In addition, infected hosts may have higher mortality than uninfected counterparts during seasonal periods when parasite transmission is halted or slowed, threatening the persistence of parasite populations. A laboratory study showed that intermediate host snails (Biomphalaria pfeifferi) commencing aestivation with more mature infections by human trematodes (Schistosoma mansoni) are 95% less likely to survive aestivation than those commencing dormancy immediately following a nascent parasite infection [10]. Similarly, in a field study, male two-spot ladybirds (Adalia bipunctata) infected by sexually transmitted mites (Coccipolipus hippodamiae) were 50% less likely to survive overwintering than uninfected males [11]. More subtle drops in parasite survival rates are seen in other infected hosts enduring seasonal dormancy [12,13]. In cases where infected hosts do survive these seasonal bouts, the viability of their parasites is often reduced; for example, human trematode cercariae (S. mansoni) shed from post-aestivated snails (B. pfeifferi) have reduced motility than those from control snails [14]. Likewise, Solomon et al. showed that aestivating snails (Trochoidea seetzenii) had lower larval load of lungworm parasites (Muellerius capillaris) than non-aestivating snails, with fewer larvae in dormant snails developing to L3 life stage due to malnourishment [15].

In contrast, harsh seasonal conditions may promote parasite growth and reproduction. Dormancy alters the nutrient requirements of hosts and can, thus, result in an increase in the availability of certain nutrients for parasites. Morelli et al. found higher parasite burdens and development rates of lungworm larvae (Troglostrongylus brevoir) infecting hibernated land snails (Cornu aspersum) than non-hibernated snails [16]. The authors suggest that the drop in glucose requirements of hibernating mollusks due to hypometabolism likely resulted in a decrease in parasite resource competition. Parasites may also benefit from host physiological stress decreasing the efficacy of the host’s immune response [17], e.g., this is seen in hibernating Brown Bears (Ursus arctos) with lower circulating innate immune cells than non-hibernating bears [18] or aestivating anurans with a weaker response to immunological challenge (phytohemagglutinin injection assay) than active counterparts [19]. Similarly, Steinmann et al. found reduced immune gene expression in overwintering honeybees (Apis mellifera) which was associated with increased susceptibility to the Deformed Wing Virus [20]. Temperature may also directly limit the capacity of immunological processes to perform due to narrow bands of thermal optima [3,21]. For example, immune processes such as broad-spectrum melanization response and phagocytosis are performed optimally in mosquitoes (Anopholes stephensi) at 18 degrees Celsius [22], below and above which mosquitoes may be more vulnerable to infections. In fact, there are species of parasites that are “cold-active” specializing on hosts enduring wintering temperatures, such as the fish bacterium Flavobacterium psychrophilum [23] or those exclusively occupying habitats of overwintering insects [24]. Seasonal variability in transmission patterns have often been associated with a high propensity for disease outbreaks [17,25], suggesting that parasites have evolved effective phenotypes to not just endure but thrive through harsh seasonal conditions.

This review discusses phenotypes of parasites that allow for persistence when hosts are enduring harsh seasonal climates, the potential consequences of a changing global climate on parasites due to temporal/spatial shifts in host adaptive behaviors, and the possibility of these seasonal harsh periods as targets for time-specific disease intervention. We consider a broad definition of parasitism based on species consuming resources from a single host individual per life stage, regardless of whether mortality is caused by that trophic interaction [26]. This includes protists, fungi, bacteria, viruses, metazoan parasites, and hymenopteran parasitoids. This definition does not discriminate by transmission strategy (vector, trophic, direct, etc.) or infection locality (endo- and ectoparasites).

Parasite strategies for persistence in harsh seasonal climates

The circannual selective pressure of harsh seasonal conditions presents few options for parasitizing species: (1) cohabitate with their current host, (2) shift to new host species with more favorable conditions, or (3) occupy structures external to hosts (Figure 1). These strategies are possible through traits that allow for persistence and maintenance of transmission cycles despite such abiotic conditions.

Figure 1. Parasite strategies for persistence through harsh seasonal conditions.

Figure 1.

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As hosts undergo seasonal adaptations due to cold temperatures (e.g., hibernation) or desiccation (e.g., aestivation), parasites have three main strategies allowing population persistence: 1) cohabitate with dormant hosts, 2) switch to a different host species that remains active, or 3) occupy structures external to their host(s). Examples of parasite phenotypes that facilitate these strategies are provided. Created with BioRender.com. Image credit to Mary Gilham Archive Project and USFWS Headquarters (CC BY 2.0).

Strategy 1: Cohabitation

A diverse group of endo- and ectoparasites cohabitate with their dormant hosts through long winters and dry seasons [12,27–32]. Parasite species undergo several life stages and often specific body morphs may be more resilient to harsh climatic conditions. While adult mites (Riccardoella limacum) that parasitize helicid land snails (Arianta arbustorum) perish through the winter season, their offspring co-hibernate as eggs attached to the lung tissue of hibernating snails [12]. Similarly, trematodes (Schistosoma douthitti) can attain maturity and produce viable eggs in a hibernating definitive host (ground squirrels, Citellus tridecemlineatus), though at slower rates than in non-hibernating squirrels [33]. Slow development rates can work in favor of the infecting agent if an elongated incubation period allows for higher availability of immunologically naïve hosts, e.g., if emergence from host dormancy coincides with birth pulses. This is seen in the Rabies Virus in hibernating big brown bats (Eptesciscus fuscus) [31], gastrointestinal nematodes (Ostertagia gruehneri) in overwintering Reindeer (Rangifer tarandus) [34], and parasitic nematodes (Elaphostrongylus rangiferi) in hibernating snails (A. arbustorum) [32]. Additionally, high density dwellings of hosts in the winter can also drive-up intraspecific transmission of density-dependent pathogens, such as the Rabies Virus in skunks (Mephitis mephitis) [35].

Strategy 2: Shift to a different host species

Parasite species that are unable to reside in their hosts through long periods of inhospitable conditions or would be subject to large dips in population numbers often require an additional host species in their life cycle or facultatively use alternative, less compatible hosts in certain years. For example, a species of intestinal helminth (Ctenotaenia marmotae) is expelled from its definitive host during hibernation, the marmot (Marmota marmota), and overwinters in an intermediate Oribate mite host [28,36].

An effective strategy of parasites in seasonally variable habitats is a complex life cycle, which allows for the utilization of at least one active and/or resource-rich host species throughout the year. One human-infecting schistosome species (Schistosoma haemotobium) reaches an annual population bottleneck in its aestivating intermediate snail host populations (Bulinus spp.) following the drying up of ephemeral ponds which snails inhabit [4]. Chronic infections of S. haemotobium in their definitive, resource-rich hosts (typically humans), however, allow for decades of potential reinfection of post-aestivating snails and their offspring once ephemeral ponds refill. Successful shifts to a different host species require successful transmission. Therefore, mechanisms of reproductive compensation may be triggered in parasites to increase the likelihood of successful transmission when a host is entering or exiting periods of stressful conditions. For example, when exposed to experimentally reduced water levels, cercariae production of a different human schistosome (S. mansoni) increased in intermediate host snails (Biomphalaria species) as compared to infected snails not subjected to this drought stress [37].

Jumping to an alternative host species can decrease the likelihood of parasite mortality in comparison with remaining in a resource-poor, dormant definitive host. However, this switch typically comes with the caveat of lowered reproductive success within an alternative host when compared to an active definitive host. For example, parasitoid wasps (Cotesia glomerata) do not co-aestivate with their definitive host, the large white butterfly (Pieris brassicae), and are theorized to shift to several potential alternative host species and experience lowered reproductive success [38,39]. Similarly, both the viral infecting agent, Wheat Streak Mosaic Virus, and its mite vector (Aceria tosichella) are typically hosted by the commercially important wheat species (Triticum aestivum) but make use of wild grasses and weeds as a “green bridge” between harvesting and planting in the early winter months [40,41].

Parasites may also make use of new host species following bouts of harsh seasonal conditions as resource-rich pockets become available. For example, Fecchio et al. found that avian haemosporidians (order Apicomplexa) in the genera Plasmodium and Haemoproteus had higher host specificity in regions with higher rainfall seasonality [25]. The authors suggest that host specialization may be selected for due to high resource competition when vector and host populations are concentrated in response to seasonal pulses of water and resources following long periods of desiccation. In fact, avian haemosporidian parasites cause relapses in chronically infected hosts triggered by seasonal increases in hormones [42]. These increases in parasitemia typically coincide with vector emergences following periods of harsh seasonal conditions. Asymptomatic chronic infections like these are maintained by haemosporidians (Plasmodium falciparum) in humans through the dry season until mosquito vectors are available [43]. This transcriptomics study demonstrated potential mechanisms such as longer circulation within each replication cycle and increased splenic clearance of infected blood cells in dry season parasites when compared to transmission season parasites.

Strategy 3: Dwellings external to hosts

Parasites may utilize weather-hardy structures that are external to their hosts through periods of harsh seasonal conditions. This is commonly seen in plant parasites infecting cultivated or native annual plants that lose their aboveground structures. For example, plant fungal parasites produce specialized resting structures, known as chasmothecia, on the leaf surface of annual plants before the aboveground structures die for the winter [44,45]. These provide a weather-hardy refuge for fungal ascospores to develop for release in the spring. In their field study, Tack & Laine found that the number of resting structures the fungal parasite produced on a plant before the winter predicted the likelihood of parasite persistence in the following spring [45].

Other examples include gastrointestinal nematodes overwintering in the fecal pats (dung) of their cattle hosts as third-stage larvae [46] and trichostrongylid parasites of sheep that can overwinter in the soil if they reach the infective stage, and moisture and temperature conditions are favorable [47]. Additionally, several species of Carnid flies overwinter in bird nests [48], facilitated by diapause [49].

Parasitism and seasonality in the face of global change

The consequences of global change on the timing and intensity of weather patterns, such as abbreviated winters [50] or drought intensification [51], have been clearly documented. These changes to climate may alter the duration of climate adaptive behaviors of hosts [52,53], which will likely have cascading effects on parasite persistence.

Global change may decrease or increase in the average number and interannual variability of unfavorable days in a year for host and parasite, driving higher or lower disease occurrence [54]. For example, the highest spring-summer prevalence of plant-fungi that overwinter in weather-hardy resting structures is documented in years with the lowest number of days below freezing [44]. Temperature changes have also stimulated year-round residency in some populations of Monarch butterflies (Danaus plexippus) [55] leading to higher disease incidence caused by a protozoan parasite (Ophryocystis elektroscirrha) than in their migratory counterparts [56]. Additionally, Yi et al. suggest that shorter generation times across a longer period of optimal conditions allows to increased transmission potential of mosquito vectors [57]. Parasite populations may instead decline due to temporal or thermal mismatches between host and parasite [3,58] or decreases in host ranges with intensifying droughts [54]. However, decreases in fitness due to host-parasite mismatches are likely to challenge parasites to adapt to global change. High population growth rates and short generation times of parasites [17] and parasite-transmitting vectors [59] are likely to promote thermal adaptation. This adaptive potential is seen in nematode lungworms (Rhabdias psuedosphaerocephala) that infect the invasive cane toad (Rhinella marina)—lungworms produce larger eggs, larvae, and adults in host populations at the edge of their geographic range than within the optimal conditions of the range [60].

Survival through “off-season” periods (such as winter or dry season) is critical to the continued transmission success of parasite species. While adaptive phenotypes allow parasites to persevere through the harsh seasonal conditions, it is often at survival rates that challenge population persistence [44]. However, with the possibility of conditions becoming more favorable for parasites with shorter “off-season” periods and longer transmission periods, there is an urgency to identify novel ways to reinforce parasite mitigation.

A call for “off-season” parasite interventions

These annual periods of population busts provide a potentially unique opportunity for the disruption of transmission cycles. Some studies do consider host phenology in guiding disease control, such as molluscicide application in the spring to target nutrient-starved wintered snails with low population sizes [61] or in lower temperatures [62]. Linske et al. also observed that the absence of insulation from snowpacks and leaf litter led to a decrease in survival of Blacklegged ticks (Ixodes scapularis) that transmit Lyme disease bacterial sp. Borrelia burgdorferi [63]. Another example is the improvement in the performance of an Anopheles vector survival model with the inclusion of an aestivation parameter [64]. More often, however, parasites during these “off-season” periods are ignored as they are difficult to sample, and peaks of infection prevalence typically occur outside of these time spans. Parasite survival during this time of population bottleneck is likely to have profound consequences on the size of population booms during peak transmission periods.

Targeting the intermediate host or vector in “off-season” periods is especially enticing as it has the potential for population declines before peak transmission periods even occur. For instance, the removal/disturbance of leaf litter and snowpacks in high Lyme disease risk areas exposed vectors to unfavorably cold conditions and significantly reduced numbers before peak parasite exposure [63]. Similar interventions may be effective in other parasite-vector systems, however, very little is known about the dormancy capabilities of vectoring species. For those that have been studied, the capacities are impressive, e.g., Lehmann et al. recaptured a single malaria-transmitting mosquito (Anopheles gambiae) from a mark-and-recapture study of 6931 mosquitoes, providing evidence that these mosquitoes can survive aestivation for up to seven months [65]. Combining a better understanding of the ecology of aestivating mosquitoes with continued destruction of larval habitats would likely lead to a more successful interruption of malaria transmission.

A similarly impressive length of aestivation is seen in schistosome transmitting snails (Bulinus spp.) leading to seasonal decreases in population numbers, especially of infected snails [4]. As these snails most often occupy human-dug and heavily used water bodies, the localities of their aestivation behavior are less elusive than mosquitoes. This presents a promising opportunity to test low-tech interventions. This could include approaches like Linske et al. that expose vectors to hostile climatic conditions [63]. Alternatively, vectors could be “tricked” into arousing from dormancy prematurely despite inhospitable climatic conditions; an extension of the “ecological trap” concept coined by Dennehy et al. [66]. In the snail-schistosome system such interventions could look like: (1) soil disturbance to expose snails to intolerable dry conditions, (2) pouring sufficient water to stimulate early arousal and subsequent mortality, and (3) covering the soil with a black tarp to increase the soil temperature above tolerability. These types of low-tech and cost-effective interventions could easily be implemented by local community members at a large geographic scale.

Concluding remarks

Harsh seasonal conditions provide a yearly test of the capacity for parasite populations to persist. While parasites have a myriad of adaptations to weather these conditions, population numbers dwindle significantly providing enticing fodder for disease control. Closer attention should be paid to parasites and/or vectors when undergoing seasonal dormancy (see Outstanding Questions). We argue that a better understanding of vector ecology and phenology could allow for low-tech solutions that bolster ongoing leaky interventions.

Outstanding Questions.

  • What localities or microsites are most important for dormancy of intermediate hosts, vectors, or parasites?

  • How do parasites balance selection pressures across active and inactive seasons?

  • What traits of hosts or parasites can predict the importance or sensitivity of seasonality?

  • Will interventions in the inactive season synergize or antagonize with traditional (active season) interventions?

  • How can we develop novel interventions for the inactive seasons?

  • As vector and intermediate host populations often have effective population recovery following bottlenecks, would these types of interventions require multiple applications?

Highlights.

  • Hosts and vectors have impressive capabilities for seasonal dormancy, with many species remaining inactive for more than half of the annual cycle.

  • Global change has impacted the duration of these climate adaptive behaviors, with the potential for temporal, spatial or thermal mismatches between host and parasite.

  • Alterations in the duration of host/vector dormancy could increase or decrease the number of favorable days for parasites, with profound impacts on disease outcomes.

  • Disease interventions are strengthened by incorporating knowledge of the phenology of vectors and intermediate hosts.

Acknowledgements

We would like to thank members of the Civitello laboratory for providing helpful comments on the manuscript that lead to this publication. NCS and DJC are supported on a National Institutes of Health / National Institute of Allergy and Infectious Diseases grant R01 AI150774.

Glossary

Aestivation

extended dormancy of an organism due to environmental desiccation, typically facilitated by slowed metabolism and water retention strategies.

Alternative host

an organism that facilitates the persistence of a parasite population during transitions where the definitive host is unavailable, often at lower parasitemia. The parasite’s life cycle can be completed without the use of this host.

Definitive host

the organism in which the parasite reaches the adult stage and reproduces sexually.

Diapause

a period of interrupted development, often due to adverse climatic conditions and typically in arthropods. Diapause is typically facilitated by metabolic depression and inactivity.

Dormancy

a period of inactivity of an organism.

Hibernation

extended dormancy of an organism due to unfavorably cold temperatures, typically facilitated by slowed metabolism, breathing and heart rate.

Intermediate host

the organism in which a parasite species is found in their immature form. A species of parasite may have more than one intermediate host. Parasites may reproduce asexually within this host.

Phenology

traits of an organism that are time-specific within the annual cycle, typically coinciding to changes in climate or photoperiod.

Footnotes

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Declaration of Interests

The authors declare no competing interests.

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