SEED: A framework for integrating ecological stoichiometry and eco‐evolutionary dynamics

Characterising the extent and sources of intraspecific variation and their ecological consequences is a central challenge in the study of eco‐evolutionary dynamics. Ecological stoichiometry, which uses elemental variation of organisms and their environment to understand ecosystem patterns and processes, can be a powerful framework for characterising eco‐evolutionary dynamics. However, the current emphasis on the relative content of elements in the body (i.e. organismal stoichiometry) has constrained its application. Intraspecific variation in the rates at which elements are acquired, assimilated, allocated or lost is often greater than the variation in organismal stoichiometry. There is much to gain from studying these traits together as components of an ‘elemental phenotype’. Furthermore, each of these traits can have distinct ecological effects that are underappreciated in the current literature. We propose a conceptual framework that explores how microevolutionary change in the elemental phenotype occurs, how its components interact with each other and with other traits, and how its changes can affect a wide range of ecological processes. We demonstrate how the framework can be used to generate novel hypotheses and outline pathways for future research that enhance our ability to explain, analyse and predict eco‐evolutionary dynamics

An experimental test of the growth rate hypothesis as a predictive framework for microevolutionary adaptation

The growth rate hypothesis (GRH) posits that the relative body phosphorus content of an organism is positively related to somatic growth rate, as protein synthesis, which is necessary for growth, requires P-rich rRNA. This hypothesis has strong support at the interspecific level. Here, we explore the use of the GRH to predict microevolutionary responses in consumer body stoichiometry. For this, we subjected populations of the rotifer Brachionus calyciflorus to selection for fast population growth rate (PGR) in P-rich (HPF) and P-poor (LPF) food environments. With common garden transplant experiments, we demonstrate that in HP populations evolution toward increased PGR was concomitant with an increase in relative phosphorus content. In contrast, LP populations evolved higher PGR without an increase in relative phosphorus content. We conclude that the GRH has the potential to predict microevolutionary change, but that its application is contingent on the environmental context. Our results highlight the potential of cryptic evolution in determining the performance response of populations to elemental limitation of their food resources

Patterns of differentiation in the life history and demography of four recently described species of the Brachionus calyciflorus cryptic species complex

1. Brachionus calyciflorus is arguably the most studied freshwater monogonont roti‐ fer. Although it has been recognised as a cryptic species complex for more than a decade, a formal (re‐)description of the four species known so far (B. calyciflorus, Brachionus dorcas, Brachionus elevatus, and Brachionus fernandoi) has only recently been made. Information on the ecology of these species is very scant and frag‐ mented. The aim of this study was to test for ecological divergence between these four species, specifically their life history strategy and population demography. 2. We conducted a life history experiment using 12–16 genotypes per species. For each species, genotypes were extracted from at least three different natural pop‐ ulations. In addition, we performed population‐level culture experiments with the aim to compare population growth rates and demographic structure of experi‐ mental populations among species. Finally, we searched the literature for life his‐ tory studies with molecular data allowing retrospective species identification. 3. We found pronounced differences in life history traits between B. fernandoi and the other three species. B. fernandoi had higher egg and juvenile development times and a lower egg production rate and mictic ratio. We detected no significant life history differences among B. calyciflorus, B. elevatus, and B. dorcas. 4. Population growth rates of B. fernandoi and B. calyciflorus were higher than those of B. elevatus and B. dorcas. Life history divergence resulted in marked differences in the demographic structure of populations. Populations of B. fernandoi con‐ tained larger fractions of pre‐reproductive females and lower fractions of adult females with sexual eggs than populations of B. calyciflorus, B. elevatus, and B. dor‐ cas. Mortality was found to be highest in B. elevatus and lowest in B. calyciflorus populations. 5. Our results show that a reverse taxonomy approach is powerful in revealing sources of variation in ecologically relevant traits of cryptic species, such as life history and demographic structure. Explicit consideration of this variation is cru‐ cial for future studies of their dynamics in natural communities. KEYWORDS ecological divergence, integrative taxonomy, monogonont rotifer, reverse taxonomy, sibling species</p

Functional diversity can facilitate the collapse of an undesirable ecosystem state

Biodiversity may increase ecosystem resilience. However, we have limited understanding if this holds true for ecosystems that respond to gradual environmental change with abrupt shifts to an alternative state. We used a mathematical model of anoxic–oxic regime shifts and explored how trait diversity in three groups of bacteria influences resilience. We found that trait diversity did not always increase resilience: greater diversity in two of the groups increased but in one group decreased resilience of their preferred ecosystem state. We also found that simultaneous trait diversity in multiple groups often led to reduced or erased diversity effects. Overall, our results suggest that higher diversity can increase resilience but can also promote collapse when diversity occurs in a functional group that negatively influences the state it occurs in. We propose this mechanism as a potential management approach to facilitate the recovery of a desired ecosystem state

An experimental test of the growth rate hypothesis as a predictive framework for microevolutionary adaptation

The growth rate hypothesis (GRH) posits that the relative body phosphorus content of an organism is positively related to somatic growth rate, as protein synthesis, which is necessary for growth, requires P-rich rRNA. This hypothesis has strong support at the interspecific level. Here, we explore the use of the GRH to predict microevolutionary responses in consumer body stoichiometry. For this, we subjected populations of the rotifer Brachionus calyciflorus to selection for fast population growth (PGR) in P-rich (HPF) and P-poor (LPF) food environments. With common garden transplant experiments, we demonstrate that in HP populations evolution towards increased PGR was concomitant with an increase in relative phosphorus content. In contrast, LP populations evolved higher PGR without an increase in relative phosphorus content. We conclude that the GRH has the potential to predict microevolutionary change, but that its application is contingent on the environmental context. Our results highlight the potential of cryptic evolution in determining the performance response of populations to elemental limitation of their food resources

Patterns of differentiation in the life history and demography of four recently described species of the Brachionus calyciflorus cryptic species complex

status: publishe

Direct and indirect effects of resource P-limitation differentially impact population growth, life history and body elemental composition of a zooplankton consumer

One of the central tenets of ecological stoichiometry is that consumer growth rate is strongly determined by food phosphorus (P) content. In planktonic organisms population growth rates of zooplankton have repeatedly been shown to be reduced when fed with P-limited algal food sources. However, P-limitation may also affect other quality-related aspects of algae, such as biochemical composition or palatability. We studied the population growth, detailed life history and body elemental composition of the herbivorous rotifer, Brachionus calyciflorus, in response to three different food quality treatments: algae cultured in high phosphorus conditions (average algal molar C:P ≈112,‘HP’), algae cultured in low P conditions (molar C:P ≈ 631, ‘LP’) and low-P cultured algae spiked with P just before feeding (molar C:P ≈113, ‘LP+P’). LP+P algae thus combined high P content with a history of growth under P-limited conditions. Total P content and the C:P ratio of rotifers in the LP+P treatment equaled those of rotifers in the HP treatment. Rotifer population growth rates were higher in HP than in LP and intermediate in the LP+P treatment. Similarly, many life history traits observed for animals in the LP+P treatment, such as somatic growth rate, age at maturity, and egg production rate were also intermediate to those observed in the LP and HP treatments. However, there were important deviations from this pattern: size at first reproduction and egg mortality in the LP+P treatment equaled the HP treatment, whereas size and development time of the first eggs equaled those of the LP treatment. Our results indicate that elemental limitation cannot fully explain reduced performance of consumers fed with P-limited algae and strongly suggest that indirect, non-stoichiometric effects of P-limitation, e.g. via changes in biochemical composition or morphology of the algae also play a major role. Furthermore, our study highlights that such indirect effects have a differential impact on major fitness components and may as such also determine the population dynamics and demographic structure of consumer populations

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

“Ecological stoichiometry,” a framework that focuses explicitly on the balances and flows of chemical elements within and between organisms and ecosystems, has provided crucial insights into many biological patterns and processes. Despite the proliferation of stoichiometrically-focused studies in recent decades and recognition of the potential for rapid evolution of stoichiometric traits, the prevalence of genetic variation in stoichiometric traits within species remains unclear. We compiled data from 30 published common garden studies of a broad range of taxa (including invertebrates, vertebrates, and autotrophs) to examine how genetic variation influences the acquisition, assimilation, allocation (AAA), composition, and excretion of elements. To quantify the extent of genetic variation for a given trait we calculated the absolute mean response ratio from pairwise comparisons of populations within the same common garden (820 population and 708 genotype comparisons). We observed substantial intraspecific variation of stoichiometric traits across populations and among genotypes; however, the magnitude of variation was greater in AAA traits (effect sizes of 20 and 164% for population and genotype contrasts, respectively) and excretion (effect sizes of 52 and 23%) than in content of carbon (2.1 and 3.1%) and nitrogen (4.5 and 24%). These results suggest that the content of some elements may be evolutionarily constrained relative to AAA traits that determine the processing of these elements, and that a sole focus on elemental content would underestimate the importance of intraspecific genetic variation, particularly within populations. Across many trait types the variation was greater among genotypes within a population than across populations. Finally, we compared pairs of populations from environments with different phosphorus (P) availability to pairs of populations with similar P availability. Genetic variation in the traits measured was similar regardless of the P environment from which genotypes were isolated, suggesting that differences in elemental availability across environments do not necessarily drive enhanced trait divergence. Overall, our results highlight the substantial amount of intraspecific variation in stoichiometric traits and underscore the potential importance of intraspecific variation in driving ecological and evolutionary processes

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

“Ecological stoichiometry,” a framework that focuses explicitly on the balances and flows of chemical elements within and between organisms and ecosystems, has provided crucial insights into many biological patterns and processes. Despite the proliferation of stoichiometrically-focused studies in recent decades and recognition of the potential for rapid evolution of stoichiometric traits, the prevalence of genetic variation in stoichiometric traits within species remains unclear. We compiled data from 30 published common garden studies of a broad range of taxa (including invertebrates, vertebrates, and autotrophs) to examine how genetic variation influences the acquisition, assimilation, allocation (AAA), composition, and excretion of elements. To quantify the extent of genetic variation for a given trait we calculated the absolute mean response ratio from pairwise comparisons of populations within the same common garden (820 population and 708 genotype comparisons). We observed substantial intraspecific variation of stoichiometric traits across populations and among genotypes; however, the magnitude of variation was greater in AAA traits (effect sizes of 20 and 164% for population and genotype contrasts, respectively) and excretion (effect sizes of 52 and 23%) than in content of carbon (2.1 and 3.1%) and nitrogen (4.5 and 24%). These results suggest that the content of some elements may be evolutionarily constrained relative to AAA traits that determine the processing of these elements, and that a sole focus on elemental content would underestimate the importance of intraspecific genetic variation, particularly within populations. Across many trait types the variation was greater among genotypes within a population than across populations. Finally, we compared pairs of populations from environments with different phosphorus (P) availability to pairs of populations with similar P availability. Genetic variation in the traits measured was similar regardless of the P environment from which genotypes were isolated, suggesting that differences in elemental availability across environments do not necessarily drive enhanced trait divergence. Overall, our results highlight the substantial amount of intraspecific variation in stoichiometric traits and underscore the potential importance of intraspecific variation in driving ecological and evolutionary processes