Trade‐offs between morphology and thermal niches mediate adaptation in response to competing selective pressures

Abstract

The effects of climate change—such as increased temperature variability and novel predators—rarely happen in isolation, but it is unclear how organisms cope with multiple stressors simultaneously. To explore this, we grew replicate Paramecium caudatum populations in either constant or variable temperatures and exposed half to predation. We then fit thermal performance curves (TPCs) of intrinsic growth rate (rmax) for each replicate population (N = 12) across seven temperatures (10°C–38°C). TPCs of P. caudatum exposed to both temperature variability and predation responded only to one or the other (but not both), resulting in unpredictable outcomes. These changes in TPCs were accompanied by changes in cell morphology. Although cell volume was conserved across treatments, cells became narrower in response to temperature variability and rounder in response to predation. Our findings suggest that predation and temperature variability produce conflicting pressures on both thermal performance and cell morphology. Lastly, we found a strong correlation between changes in cell morphology and TPC parameters in response to predation, suggesting that responses to opposing selective pressures could be constrained by trade‐offs. Our results shed new light on how environmental and ecological pressures interact to elicit changes in characteristics at both the individual and population levels. We further suggest that morphological responses to interactive environmental forces may modulate population‐level responses, making prediction of long‐term responses to environmental change challenging.

Thermal adaptation in a holobiont accompanied by phenotypic changes in an endosymbiont

“…We maintained populations in a growth (approximately exponential) phase following Uiterwaal et al. (2020). Three times a week, we inspected each population and if growth was sufficient (meaning the population consisted of about 200 cells or more, actual counts on splitting days were ∼170–1850 cells); half of the population (10 ml) was transferred to a new Petri dish and fed with an additional 10 ml of inoculated protozoan media.…”

“…Moreover, TPCs for r max can change not only from the direct impacts of predators or parasites (e.g., Padfield et al 2016) but also through behavioral or life history responses to the risk that negative interactions pose (Luhring and DeLong, 2016; Uiterwaal et al. 2020). Mutualistic interactions, such as bees and the flowers they pollinate (Shrestha et al.…”

“…Additionally, TPCs can illustrate how interactions between species are affected by temperature. Predation rates, for example, may show a unimodal response to temperature (Englund et al 2011;Uszko et al 2017;Uiterwaal et al 2020). Moreover, TPCs for r max can change not only from the direct impacts of predators or parasites (e.g., Padfield et al 2016) but also through behavioral or life history responses to the risk that negative interactions pose (Luhring and DeLong, 2016;Uiterwaal et al 2020).…”

“…Predation rates, for example, may show a unimodal response to temperature (Englund et al 2011;Uszko et al 2017;Uiterwaal et al 2020). Moreover, TPCs for r max can change not only from the direct impacts of predators or parasites (e.g., Padfield et al 2016) but also through behavioral or life history responses to the risk that negative interactions pose (Luhring and DeLong, 2016;Uiterwaal et al 2020). Mutualistic interactions, such as bees and the flowers they pollinate (Shrestha et al 2018) and endosymbionts and their hosts (Gates et al 1992), also may be affected by temperature.…”

Body size and shape responses to warming and resource competition

“…Body shape responses could therefore be important for understanding competitive abilities while the major effect of temperature on body size suggests that body size responses could be predominantly driven by metabolic demands (DeLong, 2012; Forster et al., 2012). Interactive effects of temperature and predation risk on Paramecium cell length, but not overall size (Uiterwaal et al., 2020), further highlight the role of multiple environmental drivers on size and shape.…”