Evolution of hosts paying manifold costs of defence

Cressler, Clayton E.; Graham, Andrea L.; Day, Troy

doi:10.1098/rspb.2015.0065

Cited by 45 publications

(41 citation statements)

References 44 publications

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“…Then, we compared the relative impacts of TLR-4 expression and site of capture on three costs of inflammation: energetic, nutritional and collateral damage. Each cost type has different ramifications for hosts and hence the ecology and evolution of hosts and parasites (Cressler et al, 2015). Energetic costs entail increased calorie turnover, which could impose tradeoffs with other host life functions.…”

Section: Introductionmentioning

confidence: 99%

Costs of immunity and their role in the range expansion of the house sparrow in Kenya

Martin

Kilvitis

Brace

et al. 2017

Journal of Experimental Biology

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There are at least two reasons to study traits that mediate successful range expansions. First, dispersers will found new populations and thus impact the distribution and evolution of species. Second, organisms moving into new areas will influence the fate of resident communities, directly competing with or indirectly affecting residents by spreading non-native or spilling-back native parasites. The success of invaders in new areas is likely mediated by a counterbalancing of costly traits. In new areas where threats are comparatively rare, individuals that grow rapidly and breed prolifically should be at an advantage. High investment in defenses should thus be disfavored. In the present study, we compared the energetic, nutritional and collateral damage costs of an inflammatory response among Kenyan house sparrow (Passer domesticus) populations of different ages, asking whether costs were related to traits of individuals from three different capture sites. Kenya is among the world's most recent range expansions for this species, and we recently found that the expression of Toll-like receptors (TLRs), leukocyte receptors that instigate inflammatory responses when bound to microbial elements, was related to the range expansion across the country. Here, we found (contrary to our expectations) that energetic and nutritional costs of inflammation were higher, but damage costs were lower, in range-edge compared with core birds. Moreover, at the individual level, TLR-4 expression was negatively related to commodity costs (energy and a critical amino acid) of inflammation. Our data thus suggest that costs of inflammation, perhaps mediated by TLR expression, might mitigate successful range expansions.

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Section: Introductionmentioning

confidence: 99%

Costs of immunity and their role in the range expansion of the house sparrow in Kenya

Martin

Kilvitis

Brace

et al. 2017

Journal of Experimental Biology

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“…Optimal investment in microbe‐independent and sensitive inducible dynamics is also likely to depend on the frequency and predictability of parasite exposure, complementing predictions made for optimal investment in constitutive and inducible immunity (Hamilton et al, ; Mayer et al, ). Finally, epidemiological feedbacks in populations with different immune strategy distributions should lead to different pressures on transmission and virulence (Cressler et al, ), further creating an opportunity for natural variation in both microbe dependent and independent terms.…”

Section: Discussionmentioning

confidence: 99%

“…The parasites to which hosts are exposed, the frequency of exposure, and the costs and benefits associated with mounting defences against those parasites, are all expected to contribute to the evolution of inducible immune responses (Cressler et al, 2015;Frank, 2002;Hamilton et al, 2008;Mayer, Mora, Rivoire, & Walczak, 2016). The dynamics of immunity during the acute infection phase are particularly important for host fitness, as modest levels of variation in early responses could lead to drastic variation in host mortality and parasite persistence (Duneau et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

“…A mathematical model created by Hamilton, Siva-Jothy, and Boots (2008) suggests that highly predictable parasite growth rates should always favour modulation of constitutive investment, whereas variation or unpredictability in parasite growth rates should favour a combination of constitutive and inducible investment. Other models add to these predictions by suggesting that longer inducible time delays (Shudo & Iwasa, 2001) and developmental constraints on inducible immune investment (Tate & Graham, 2015a) should further favour constitutive defence, while variation in the types of costs associated with constitutive and inducible responses could favour differential investment in recovery rates after infection (Cressler, Graham, & Day, 2015).…”

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confidence: 99%

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Natural variation in the contribution of microbial density to inducible immune dynamics

et al. 2019

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Immune responses evolve to balance the benefits of microbial killing against the costs of autoimmunity and energetic resource use. Models that explore the evolution of optimal immune responses generally include a term for constitutive immunity, or the level of immunological investment prior to microbial exposure, and for inducible immunity, or investment in immune function after microbial challenge. However, studies rarely consider the functional form of inducible immune responses with respect to microbial density, despite the theoretical dependence of immune system evolution on microbe‐ versus immune‐mediated damage to the host. In this study, we analyse antimicrobial peptide (AMP) gene expression from seven wild‐caught flour beetle populations (Tribolium spp.) during acute infection with the virulent bacteria Bacillus thuringiensis (Bt) and Photorhabdus luminescens (P.lum) to demonstrate that inducible immune responses mediated by the humoral IMD pathway exhibit natural variation in both microbe density‐dependent and independent temporal dynamics. Beetle populations that exhibited greater AMP expression sensitivity to Bt density were also more likely to die from infection, while populations that exhibited higher microbe density‐independent AMP expression were more likely to survive P. luminescens infection. Reduction in pathway signalling efficiency through RNAi‐mediated knockdown of the imd gene reduced the magnitude of both microbe‐independent and dependent responses and reduced host resistance to Bt growth, but had no net effect on host survival. This study provides a framework for understanding natural variation in the flexibility of investment in inducible immune responses and should inform theory on the contribution of nonequilibrium host‐microbe dynamics to immune system evolution.

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“…Codiversification is particularly expected for endoparasites (more than for ectoparasites) given their direct interaction with the host immune system (Poinar ; Poulin ; Cressler et al. , ). Here, we report on endoparasitic nematodes which infect different species of stick insects in the genus Timema .…”

Section: Introductionmentioning

confidence: 99%

Nematode endoparasites do not codiversify with their stick insect hosts

Larose

Schwander

2016

Ecology and Evolution

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Host–parasite coevolution stems from reciprocal selection on host resistance and parasite infectivity, and can generate some of the strongest selective pressures known in nature. It is widely seen as a major driver of diversification, the most extreme case being parallel speciation in hosts and their associated parasites. Here, we report on endoparasitic nematodes, most likely members of the mermithid family, infecting different Timema stick insect species throughout California. The nematodes develop in the hemolymph of their insect host and kill it upon emergence, completely impeding host reproduction. Given the direct exposure of the endoparasites to the host's immune system in the hemolymph, and the consequences of infection on host fitness, we predicted that divergence among hosts may drive parallel divergence in the endoparasites. Our phylogenetic analyses suggested the presence of two differentiated endoparasite lineages. However, independently of whether the two lineages were considered separately or jointly, we found a complete lack of codivergence between the endoparasitic nematodes and their hosts in spite of extensive genetic variation among hosts and among parasites. Instead, there was strong isolation by distance among the endoparasitic nematodes, indicating that geography plays a more important role than host‐related adaptations in driving parasite diversification in this system. The accumulating evidence for lack of codiversification between parasites and their hosts at macroevolutionary scales contrasts with the overwhelming evidence for coevolution within populations, and calls for studies linking micro‐ versus macroevolutionary dynamics in host–parasite interactions.

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Evolution of hosts paying manifold costs of defence

Cited by 45 publications

References 44 publications

Costs of immunity and their role in the range expansion of the house sparrow in Kenya

Costs of immunity and their role in the range expansion of the house sparrow in Kenya

Natural variation in the contribution of microbial density to inducible immune dynamics

Nematode endoparasites do not codiversify with their stick insect hosts

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