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

Abstract

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 Qst/Fst 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.

Keywords: Qst/Fst; common garden experiment; ectoparasites; generalism; pre-adaptation; thermal reaction norms.

Figure 1.

Populations of the parasite Tracheliastes polycolpus sampled in southwestern France. (a) Representation of mean monthly water temperature (±s.d.) for each river sampled, from April 2014 to October 2014. (b) Map of the six sampled rivers and their affiliation to the two genetic clusters (northern and southern clusters). Black circles indicate the sampling sites of T. polycolpus from the northern cluster; grey circles indicate the sampling sites of the southern cluster.

Figure 2.

Survival reaction norms of Tracheliastes polycolpus larvae exposed to three different experimental temperatures (16°C, 19°C, 22°C). (a) Representation of the mean survival time (±s.e.) of individuals from the six rivers sampled. (b) Representation of the survival reaction norms of individuals from the two genetic clusters: northern cluster (Célé, Viaur, Dadou) and southern cluster (Arize, Volp, Salat).

Figure 3.

Representation of difference in survival time of Tracheliastes polycolpus between pairs of experimental treatments for each river according to the mean annual temperature in each river sampled. Black circles represent the differences between 19°C and 16°C treatments for each river, the background grey diamonds represent the differences between 22°C and 19°C treatments, and grey squares the differences between 22°C and 16°C treatments. Solid black lines indicate the regression slope for 19°C and 16°C differences, and dashed grey lines indicate the regression slope for 22°C and 19°C differences, and 22°C and 16°C treatments.

Figure 4.

Comparison of quantitative (Q_st, dots) and neutral (F_st, horizontal dashed lines) genetic differentiations among T. polycolpus populations. (a) Comparisons for quantitative traits (survival time) measured at each experimental temperature (survival times at 16°C, white dots; survival times at 19°C, grey dots; survival times at 22°C, black dots), and (b) comparisons for quantitative traits (differences in survival time) measured between each experimental temperature (difference in survival times between 16°C and 19°C, white dots; difference in survival times between 19°C and 22°C, grey dots; difference in survival times between 16°C and 22°C, black dots). In both (a,b), comparisons are performed for all six populations from the two genetic clusters (all genetic clusters), the three populations from the southern cluster, or the three populations from the northern cluster. The 95% CIs are the vertical lines for the Q_st and the grey areas for the F_st. When 95% CIs of Q_st and F_st do not overlap, this indicates significant differences between Q_st and F_st, which are denoted as double asterisks. n.s. indicates not significant when the 95% CIs overlap.