Fluctuating Temperature Leads to Evolution of Thermal Generalism and Preadaptation to Novel Environments

Ketola, Tarmo; Mikonranta, Lauri; Zhang, Ji; Saarinen, Kati; Örmälä, Anni-Maria; Friman, Ville‐Petri; Mappes, Johanna; Laakso, Jouni

doi:10.1111/evo.12148

Cited by 91 publications

(230 citation statements)

References 68 publications

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“…It is noteworthy that theories about specialism/generalism trade‐off are highly idealized and a “Jack of all temperatures” does not always have to be a master of none (Angilletta, 2009). Genotypes can have broader thermal performance range without always paying a visible performance cost at optimum conditions, but possibly involving a trade‐off with other traits (Huey & Hertz, 1984; Ketola et al., 2013), such as virulence (Ketola et al., 2013; Sturm et al., 2011). For environmentally growing opportunist pathogens, adaptations for more efficient exploitation of one growth environment could be expected to cause repercussions in their ability to grow in the other environment (Brown et al., 2012), such as host environment.…”

Section: Discussionmentioning

confidence: 99%

“…This could explain why more generalist strains with broader thermal performance breadth were less virulent than strains with narrower TPB (see: PC1 effect in Table 3 and Figure 4a). Similarly, expression of virulence factors was found to decrease outside‐host growth rate in Salmonella typhimurium (Sturm et al., 2011) and adaptation to tolerate thermal fluctuations and protozoan predators have caused lowered virulence in experimental evolution settings with microbial pathogens (Friman et al., 2011; Ketola et al., 2013; Mikonranta et al., 2012; Zhang et al., 2014). …”

Section: Discussionmentioning

confidence: 99%

“…The growth curves were analysed as described in Ketola et al. (2013) to estimate maximum growth rate and maximum biomass yield. Maximum yield is estimated from the plateau phase of a growth curve while maximum growth rate is estimated from its early phase and is thus influenced by the potentially large relative noise in the OD measurement during this phase.…”

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Broad thermal tolerance is negatively correlated with virulence in an opportunistic bacterial pathogen

Ashrafi

Bruneaux

Sundberg

et al. 2018

Evolutionary Applications

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Predicting the effects of global increase in temperatures on disease virulence is challenging, especially for environmental opportunistic bacteria, because pathogen fitness may be differentially affected by temperature within and outside host environment. So far, there is very little empirical evidence on the connections between optimal temperature range and virulence in environmentally growing pathogens. Here, we explored whether the virulence of an environmentally growing opportunistic fish pathogen, Flavobacterium columnare, is malleable to evolutionary changes via correlated selection on thermal tolerance. To this end, we experimentally quantified the thermal performance curves (TPCs) for maximum biomass yield of 49 F. columnare isolates from eight different geographic locations in Finland over ten years (2003–2012). We also characterized virulence profiles of these strains in a zebra fish (Danio rerio) infection model. We show that virulence among the strains increased over the years, but thermal generalism, and in particular tolerance to higher temperatures, was negatively associated with virulence. Our data suggest that temperature has a strong effect on the pathogen genetic diversity and therefore presumably also on disease dynamics. However, the observed increase in frequency and severity of F. columnare epidemics over the last decade cannot be directly linked to bacterial evolution due to increased mean temperature, but is most likely associated with factors related to increased length of growing season, or other time‐dependent change in environment. Our study demonstrates that complex interactions between the host, the pathogen and the environment influence disease virulence of an environmentally growing opportunistic pathogen.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Broad thermal tolerance is negatively correlated with virulence in an opportunistic bacterial pathogen

Ashrafi

Bruneaux

Sundberg

et al. 2018

Evolutionary Applications

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“…Local adaptation, genetic drift and founder effects are processes that can all generate population variation (both on mean values and reaction norms) in important traits such as thermal tolerance [8]. For instance, populations currently living in environments with high temperature fluctuations may evolve thermal generalism, whereas populations living in stable environments should evolve thermal specialization towards the local optima [9]. We can expect generalist populations to better cope with future climate change [9].…”

Section: Introductionmentioning

confidence: 99%

“…For instance, populations currently living in environments with high temperature fluctuations may evolve thermal generalism, whereas populations living in stable environments should evolve thermal specialization towards the local optima [9]. We can expect generalist populations to better cope with future climate change [9]. Thus, rather than considering a species as a uniform entity, this hypothesis considers a species as a heterogeneous entity that may include population subsets that would better fit future climate change [7].…”

Section: Introductionmentioning

confidence: 99%

Local adaptation drives thermal tolerance among parasite populations: a common garden experiment

et al. 2016

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Understanding the evolutionary responses of organisms to thermal regimes is of prime importance to better predict their ability to cope with ongoing climate change. Although this question has attracted interest in free-living organisms, whether or not infectious diseases have evolved heterogeneous responses to climate is still an open question. Here, we ran a common garden experiment using the fish ectoparasite Tracheliastes polycolpus, (i) to test whether parasites living in thermally heterogeneous rivers respond differently to an experimental thermal gradient and (ii) to determine the evolutionary processes (natural selection or genetic drift) underlying these responses. We demonstrated that the reaction norms involving the survival rate of the parasite larvae (i.e. the infective stage) across a temperature gradient significantly varied among six parasite populations. Using a Q st /F st approach and phenotype -environment associations, we further showed that the evolution of survival rate partly depended upon temperature regimes experienced in situ, and was mostly underlined by diversifying selection, but also-to some extent-by stabilizing selection and genetic drift. This evolutionary response led to population divergences in thermal tolerance across the landscape, which has implications for predicting the effects of future climate change.

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Rapid evolutionary adaptation to elevated salt concentrations in pathogenic freshwater bacteria Serratia marcescens

Ketola

Hiltunen

2014

Ecology and Evolution

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Rapid evolutionary adaptions to new and previously detrimental environmental conditions can increase the risk of invasion by novel pathogens. We tested this hypothesis with a 133-day-long evolutionary experiment studying the evolution of the pathogenic Serratia marcescens bacterium at salinity niche boundary and in fluctuating conditions. We found that S. marcescens evolved at harsh (80 g/L) and extreme (100 g/L) salt conditions had clearly improved salt tolerance than those evolved in the other three treatments (ancestral conditions, nonsaline conditions, and fluctuating salt conditions). Evolutionary theories suggest that fastest evolutionary changes could be observed in intermediate selection pressures. Therefore, we originally hypothesized that extreme conditions, such as our 100 g/L salinity treatment, could lead to slower adaptation due to low population sizes. However, no evolutionary differences were observed between populations evolved in harsh and extreme conditions. This suggests that in the study presented here, low population sizes did not prevent evolution in the long run. On the whole, the adaptive potential observed here could be important for the transition of pathogenic S. marcescens bacteria from human-impacted freshwater environments, such as wastewater treatment plants, to marine habitats, where they are known to infect and kill corals (e.g., through white pox disease).

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Fluctuating Temperature Leads to Evolution of Thermal Generalism and Preadaptation to Novel Environments

Cited by 91 publications

References 68 publications

Broad thermal tolerance is negatively correlated with virulence in an opportunistic bacterial pathogen

Broad thermal tolerance is negatively correlated with virulence in an opportunistic bacterial pathogen

Local adaptation drives thermal tolerance among parasite populations: a common garden experiment

Rapid evolutionary adaptation to elevated salt concentrations in pathogenic freshwater bacteria Serratia marcescens

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