The importance of inter‐individual variation in predicting species' responses to global change drivers

Abstract

Inter‐individual variation in phenotypic traits has long been considered as “noise” rather than meaningful phenotypic variation, with biological studies almost exclusively generating and reporting average responses for populations and species’ average responses. Here, we compare the use of an individual approach in the investigation of extracellular acid–base regulation by the purple sea urchin Paracentrotus lividus challenged with elevated p CO 2 and temperature conditions, with a more traditional approach which generates and formally compares mean values. We detected a high level of inter‐individual variation in acid–base regulation parameters both within and between treatments. Comparing individual and mean values for the first (apparent) dissociation constant of the coelomic fluid for individual sea urchins resulted in substantially different (calculated) acid–base parameters, and models with stronger statistical support. While the approach using means showed that coelomic p CO 2 was influenced by seawater p CO 2 and temperature combined, the individual approach indicated that it was in fact seawater temperature in isolation that had a significant effect on coelomic p CO 2 . On the other hand, coelomic [HCO 3 − ] appeared to be primarily affected by seawater p CO 2 , and less by seawater temperature, irrespective of the approach adopted. As a consequence, we suggest that individual variation in physiological traits needs to be considered, and where appropriate taken into account, in global change biology studies. It could be argued that an approach reliant on mean values is a “procedural error.” It produces an artefact, that is, a population's mean phenotype. While this may allow us to conduct relatively simple statistical analyses, it will not in all cases reflect, or take into account, the degree of (physiological) diversity present in natural populations.

Synthesis of Thresholds of Ocean Acidification Impacts on Echinoderms

“…Given this reason, and the fact that the response was strongly linear (LSR p < 0.001, R 2 = 0.81, F = 167, DF = 40), the panel placed the extracellular fluid pH threshold at a lower pH = 7.60 (7-day duration), an LSRpredicted value 42% below the experimental control (Table 1) and low evidence. The panel noted that the buffering capacity is highly species-specific (Calosi et al, 2013a), varying among individuals within a species (Guscelli et al, 2019) and can take up to 6-12 months for a species to regain its initial acid-base status (Spicer, unpubl.). Data on rates of aerobic metabolism came from four studies (Table 2) of brittle stars (A. filiformis, O. ophiura, O. schayeri, and O. sericeum), and were normalized using control values to facilitate study comparisons (Wood et al, 2008(Wood et al, , 2010(Wood et al, , 2011Christensen et al, 2011).…”

“…Third, potentially the largest knowledge gap, relates to the need to consideration of OA with other stressors, that can potentially act as modulators for OA thresholds. Sufficient evidence exists to show that combinations of multiple stressors can change the magnitude and the direction of single, univariate stressors (Christensen et al, 2011;Wood et al, 2011;Guscelli et al, 2019). However, there is still a considerable lack of experimental data that included treatments of OA with variable temperature and DO, which precluded consideration of how to incorporate multiple stressors into the OA thresholds.…”

Environment‐driven shifts in interindividual variation and phenotypic integration within subnetworks of the mussel transcriptome and proteome

“…Even within a single generation (i.e., before evolutionary processes can act), physiological plasticity expressed differently among individuals can change the apparent correlation between genetic variation and variation in phenotype (Crawford & Oleksiak, 2007; Gibert et al, 2019). Such plasticity‐driven shifts in phenotypic variation may alter the effects of selection, thereby influencing predicted responses to environmental change (Ghalambor et al, 2007; Guscelli et al, 2019; Oleksiak & Crawford, 2012). However, environment‐driven shifts in phenotypic variation remain understudied.…”

Microhabitat temperature variation combines with physiological variation to enhance thermal resilience of the intertidal musselMytilisepta virgata

“…Another commonly overlooked type of physiological variation is the inter-individual variation in thermal tolerance found among conspecifics at a common site, where thermal conditions would be similar for all individuals (for exceptions, see: Dowd et al, 2015;Jimenez et al, 2015). The inter-individual variation of this type that has been noted in several studies of intertidal species (Dong et al, 2014;Reveillon et al, 2019) can potentially buffer the impact of thermal stress, because more thermally tolerant individuals may be capable of surviving the harshest environmental conditions (Bennett et al, 2019;Guscelli et al, 2019). As we illustrate in the present study, physiological variations, including spatial-temporal physiological performance variations and inter-individual physiological variations should be considered for evaluating thermal sensitivity in the face of change in temperature, notably in the context of global warming.…”