As Lotka notes, the most fundamental building blocks of life are elements. Ecological supply of elements sets evolutionary constraints and opens evolutionary doors. Because biology plays a critical role in the cycling of elements in the biosphere, changes in the kinetics of elements between the environment and individuals in both physiological as well as evolutionary time should feedback to alter elemental supply. Our research aims to understand the links among elemental supply, physiological and evolutionary responses, and resultant impact of such responses on elemental supply. Our research requires strong foundations in biogeochemistry and ecosystem ecology, as well as nutritional physiology and evolutionary biology. Explicit attention to elemental information across levels of organization using advances in high throughput data generation allows us to apply first principles to make cross-disciplinary inferences with unrivaled rigor. 









Left: Schematic representation of the mass-balance-based elemental framework proposed for a single element and a single genotype. Based on first principles, the concentration of an element in an individual is a function of acquisition, assimilation, and allocation of the element. The excretion (i.e. unused or waste) of this element can be predicted applying mass balance. Note that this framework applies to all of the ~25 elements represented in biology (Right; grey squares).
 
The supply of the 25 elements involved in biology represents a precisely quantifiable environment on which phenotypic evolution happens. The acquisition and assimilation of elements from the environment, and allocation of elements within the body represent genomic capabilities of individuals that determine their elemental content, while the unused elements are released back into the environment, representing a fundamental ecological function. Together, these traits are referred to as the elemental phenotype (i.e. the elemental content and processing of the 25 elements required for life, with the content and processing of each element representing an elemental trait). I test and refine this abstract model primarily using freshwater crustaceans Daphnia, although this model is applicable to any taxa. 
Physiological considerations: Prior work had found that when supply of an element (e.g., P) is below demand, daphniids increase acquisition (compensatory feeding), assimilation, and retention of P, thereby lowering excretion. Further, we illuminated the complex mechanisms underlying such responses. Using transcriptomic methods we discovered that under P limited conditions (similar to clear, oligotrophic lakes) daphniids differentially expressed about 25% of their genes. Furthermore, P limited daphniids had as much as 4 times more transcripts globally compared to P replete daphniids. Such upregulation of genes involved in widespread metabolic pathways indicated that P supply should also alter the demand and use of the other ~24 elements represented in biology, with unique ecological ramifications. 

Evolutionary considerations: We have found substantial genetic variation in elemental traits using laboratory-reared genotypes of Daphnia. We directly assessed the role of altered phosphorus in driving microevolutionary shifts in natural Daphnia populations. We exploited the unique biology of Daphnia, which produce dormant eggs preserved in lake sediments for centuries and found that these populations have undergone dramatic shifts in their population genetic structure since European settlement. Further, radiotracer assays on genotypes hatched from eggs as old as ~700 years, indicated that 700-yr-old genotypes were 40% more efficient in P utilization compared to 20-yr-old genotypes. The magnitude of this difference is substantially greater than standing genetic variation for this trait in a population. Furthermore, we have illuminated the transcriptomic basis of variation in P utilization among ancient and extant genotypes. We are developing genomic markers for P use in a recently funded NSF grant (2013-2016) to test whether these markers are correlated with trophic status of a lake (both among lakes, and within a lake using genomic sequences from dormant eggs). This work will, at minimum, reveal genomic regions of major effect that have played a role in the striking shifts in P use traits driven by eutrophication, and perhaps the nucleotides that determine key ecological functions of individuals.  

Ecological considerations: Daphnia play an important role in the cycling of elements in lakes. Invoking first principles of mass balance, observed genetic variation and/or evolutionary shifts in the ionome should alter the resupply of elements exhibiting genetic, environmental, or GxE effects. We have already established that such differences feedback to alter the quality and quantity of algae in microcosms. Specifically, we found that algae coexisting with extant (P-inefficient) genotypes grew significantly slower compared to those with ancient genotypes, particularly in high phosphorus conditions. Furthermore, we know that Daphnia genotypes differing in P use physiology affects the fitness of two Chlamydomonas genotypes that differ in P use physiology. It is likely that such results are not only driven by P use, but also variation in several other elemental traits encompassing the elemental phenotype. 
Our work illuminates some of the mechanisms behind Lotka’s poetic musing almost a century ago. Specifically, (i) ionomes are tied together with their elemental environment by physiological processes, (ii) such physiological processes are orchestrated by genomic capabilities that can evolve, (iii) shifts in the ionome due to physiological or evolutionary processes should alter the elemental environment, and (iv) such alterations should feedback to affect fitness functions of genotypes varying in the ionome, or the elemental phenotype. The fact that we are proposing such a logically consistent, and empirically verifiable notion in 2014 highlights our poor understanding of biodiversity at the most fundamental level of organization – atoms of biologically relevant elements. It is evident that elemental traits vary by several orders of magnitude even among closely related taxa. We know nothing about the physiological, ecological, and evolutionary mechanisms that underlie such striking variation/diversification (at least compared to our understanding of variation/diversification of smaller magnitude in traditional biological traits). 

In Lotka’s vein, there is much left to do to capture the spirit of the most complex drama known to mankind. Come join us in this pursuit!
Overview
“For the drama of life is like a puppet show in which stage, scenery, actors and all are made of the same stuff...so the stage and players are bound together...to catch the spirit of the piece, our attention must not all be absorbed in the players alone, but must extend also to the stage, of which they are born, on which they play their part, and with which, in a short while, they merge again.” 
                                                                                                                                         - Alfred J. Lotka (1925).