Ionome and elemental transport kinetics shaped by parallel evolution in threespine stickleback

Abstract

Evidence that organisms evolve rapidly enough to alter ecological dynamics necessitates investigation of the reciprocal links between ecology and evolution. Data that link genotype to phenotype to ecology are needed to understand both the process and ecological consequences of rapid evolution. Here, we quantified the suite of elements in individuals (i.e., ionome) and differences in the fluxes of key nutrients across populations of threespine stickleback. We find that allelic variation associated with freshwater adaptation that controls bony plating is associated with changes in the ionome and nutrient recycling. More broadly, we find that adaptation of marine stickleback to freshwater conditions shifts the ionomes of natural populations and populations raised in common gardens. In both cases ionomic divergence between populations was primarily driven by differences in trace elements rather than elements typically associated with bone. These findings demonstrate the utility of ecological stoichiometry and the importance of ionome‐wide data in understanding eco‐evolutionary dynamics.

Phosphorus limitation does not drive loss of bony lateral plates in freshwater stickleback (Gasterosteus aculeatus)

“…This alternative hypothesis is consistent with the observation that phosphorus excretion rates are not inversely related to body phosphorus content in the wild, as is expected under limiting dietary phosphorus conditions (Durston and El‐Sabaawi 2019; Rudman et al. 2019).…”

“…Interestingly, a recent study of stickleback ionomes found that rare elements, particularly barium, differ consistently between marine and freshwater fish and their native habitats (Rudman et al. 2019). This might be a factor to test in future studies, given the lack of conclusive empirical support for either calcium or phosphorus limitation driving selection for the low‐plated phenotype in freshwater.…”

“…2019), stickleback can likely meet their calcium demands by adjusting calcium uptake (Rudman et al. 2019). In contrast, fish must obtain a substantial portion of phosphorus from their diets (Vielma and Lall 1998; Avila et al.…”

Stoichiometric Traits Vary Widely Within Species: A Meta-Analysis of Common Garden Experiments

“…Using a strict definition of eco-evolutionary feedback (Schoener, 2011), two interacting processes would be required: ES traits would have to evolve rapidly in a population and the evolution of these ES traits would need to modify the environment in a way that significantly affects selection on that population. The potential for eco-evolutionary feedbacks mediated by the evolution of ES traits has been much discussed (Jeyasingh et al, 2014;Leal et al, 2017b;Rudman et al, 2019), and some studies have demonstrated that rapid evolution can shape elemental availability (Bassar et al, 2010;Rudman and Schluter, 2016). Yet, whether these differences in elemental availability feed back onto rapid evolution is wholly unknown.…”

“…These experiments minimize the effects of the environmental factors by comparing genetically distinct individuals within a common "garden" environment, thus allowing for the quantification of genetic variation either within or between populations (Lynch and Walsh, 1998). Synthesis of such studies could illuminate whether genetic variation is present, the relative amount of genetic variation within and across populations, which stoichiometric traits show genetic variation, and whether elemental limitation could influence evolution in nature (Elser, 2006;Leal et al, 2017a;Rudman et al, 2019).…”