Integrating patterns of thermal tolerance and phenotypic plasticity with population genetics to improve understanding of vulnerability to warming in a widespread copepod

Abstract

Differences in population vulnerability to warming are defined by spatial patterns in thermal adaptation. These patterns may be driven by natural selection over spatial environmental gradients, but can also be shaped by gene flow, especially in marine taxa with high dispersal potential. Understanding and predicting organismal responses to warming requires disentangling the opposing effects of selection and gene flow. We begin by documenting genetic divergence of thermal tolerance and developmental phenotypic plasticity. Ten populations of the widespread copepod Acartia tonsa were collected from sites across a large thermal gradient, ranging from the Florida Keys to Northern New Brunswick, Canada (spanning over 20° latitude). Thermal performance curves (TPCs) from common garden experiments revealed local adaptation at the sampling range extremes, with thermal tolerance increasing at low latitudes and decreasing at high latitudes. The opposite pattern was observed in phenotypic plasticity, which was strongest at high latitudes. No relationship was observed between phenotypic plasticity and environmental variables. Instead, the results are consistent with the hypothesis of a trade-off between thermal tolerance and the strength of phenotypic plasticity. Over a large portion of the sampled range, however, we observed a remarkable lack of differentiation of TPCs. To examine whether this lack of divergence is the result of selection for a generalist performance curve or constraint by gene flow, we analyzed cytochrome oxidase I mtDNA sequences, which revealed four distinct genetic clades, abundant genetic diversity, and widely distributed haplotypes. Strong divergence in thermal performance within genetic clades, however, suggests that the pace of thermal adaptation can be relatively rapid. The combined insight from the laboratory physiological experiments and genetic data indicate that gene flow constrains differentiation of TPCs. This balance between gene flow and selection has implications for patterns of vulnerability to warming. Taking both genetic differentiation and phenotypic plasticity into account, our results suggest that local adaptation does not increase vulnerability to warming, and that low-latitude populations in general may be more vulnerable to predicted temperature change over the next century.

Surviving heatwaves: thermal experience predicts life and death in a Southern Ocean diatom

“…Accumulated stress beyond a critical threshold results in mortality due to the degradation of cellular components and disruption of physiological functioning (Feijão et al, 2018, Lesser, 2006, Magozzi & Calosi, 2015, Schroda et al, 2015. Although exposure to nonlethal temperatures can also increase tolerance to further stress in some marine organisms (Clapp et al, 1997, Magozzi & Calosi, 2015, Sasaki & Dam, 2019, we do not find evidence for this in our experiment. Instead, we find that experimental populations grown at 5.8 o C (above Topt) prior to heatwave exposure had higher levels of mortality than those grown at 2.5 o C (below Topt), in both the heatwave and control treatments.…”

“…In phytoplankton, acclimation can alter organismal fitness in the new environment over several asexual generations, and is reversible if the environmental cue stops (Anning et al, 2001, Brand et al, 1981, Kremer et al, 2018. Across a wide variety of marine taxa, numerous studies have demonstrated that previous acclimation to elevated temperatures can enhance tolerance (heat hardening) when exposed to thermal extremes (Hughes et al, 2019, Magozzi & Calosi, 2015, Pansch et al, 2018, Sasaki & Dam, 2019, Scharf et al, 2015, Stuhr et al, 2017.…”

Genetic differentiation underlies seasonal variation in thermal tolerance, body size, and plasticity in a short‐lived copepod

“…In addition to the temperature and salinity measurements made at the time of collection, we also estimated the thermal environment experienced by individuals during development, as this has been shown to strongly influence thermal tolerance in adult copepods (Pereira et al., 2017; Sasaki & Dam, 2019). However, like other copepods, Acartia species exhibit an exponential relationship between temperature and development time (Kleppel et al., 1996; Mauchline, 1998; Miller et al., 1977; Peterson, 2001).…”

“…For these collections, both mature females and males were sorted into filtered seawater, which was then slowly brought to 18°C. We chose this temperature because it represents an approximate mean temperature experienced by Acartia tonsa during its growth season, and because Acartia tonsa individuals from a wide range of thermal environments have been shown to survive and reproduce at this temperature (Sasaki & Dam, 2019). Cultures were kept at ambient CO 2 concentrations.…”

Surviving Heatwaves: Thermal Experience Predicts Life and Death in a Southern Ocean Diatom

“…In phytoplankton, acclimation can alter organismal fitness in the new environment over several asexual generations, and is reversible if the environmental cue stops (Brand et al, 1981;Anning et al, 2001;Kremer et al, 2018). Across a wide variety of marine taxa, numerous studies have demonstrated that previous acclimation to elevated temperatures can enhance tolerance (heat hardening) when exposed to thermal extremes (Magozzi and Calosi, 2015;Scharf et al, 2015;Stuhr et al, 2017;Pansch et al, 2018;Hughes et al, 2019;Sasaki and Dam, 2019).…”