High altitude adaptation in the deer mouse

The summit of Mt. Evans, Colorado

Organisms living in extreme environments are excellent models for studying the mechanistic basis of evolutionary adaptation. My work with Zac Cheviron explores the physiology, genetics, and functional genomics of adaptation to high altitude environments, which are characterized by extremes in hypoxia and cold.

Small, winter active mammals living at high altitude are faced with a double bind: sustained aerobic heat generation (thermogenesis) is necessary for survival during prolonged periods of cold stress, but is severely impaired under the metabolism-suppressing conditions of hypobaric hypoxia. As such, strong directional selection on thermogenesis has been identified in high altitude populations of the deer mouse (Peromyscus maniculatus).

By comparing low- and high- altitude populations of deer mouse in field and laboratory experiments, my work in the Cheviron lab is aimed at understanding how the physiological and functional genomic mechanisms of shivering and non-shivering strategies contribute to the adaptive enhancement of thermogenesis under hypoxic stress.

This work is in collaboration with Jay Storz, Grant McClelland, Graham Scott, and Amina Qutub.

Evolution of osmoregulation in the alewife

This work is the collaborative effort of many amazing people, including Eric Schultz (my PhD advisor) and Steve McCormick.

A juvenile alewife. Photo by Kai Webler

The invasion of freshwater from the sea is among the most important evolutionary transitions in animal history, leading to diversification and adaptive radiation. Adaptations that enable such transitions are poorly understood, but likely involve evolution of osmoregulatory systems, which enable animals to maintain ion and water balance. Using the alewife (Alosa pseudoharengus) as a model system, I take an experimental approach to understanding how osmoregulatory function evolves to permit the transition into freshwater. Dams in coastal Connecticut have blocked the anadromous migrations of alewives, resulting in multiple, independently derived landlocked populations that are restricted to freshwater. This is an ideal system to explore the ways in which osmotic niche shifts alter osmoregulatory function.

We have found that adaptation to freshwater involves considerable evolutionary changes to the osmoregulatory system. Short-term experiments reveal that juvenile landlocked alewives have greatly reduced seawater tolerance and impaired osmotic balance compared to anadromous alewives (Velotta et al 2014 Oecologia). Longer-term laboratory salinity challenge experiments show that landlocked alewives also have greater tolerance of low-ion freshwater, suggesting that the evolution of freshwater tolerance is driven by a trade-off in osmoregulatory function. Our research is among the first to provide evidence that adaptation to freshwater is achieved, in part, by increases in physiological function in freshwater that come at a cost to seawater function.

An excised alewife gill
An excised alewife gill taken after salinity exposure experiments for measurement of activity and expression of ion transporters

Molecular mechanisms of adaptation to freshwater

In addition to experimentally testing physiological responses, we use salinity challenge experiments to reveal what molecular mechanisms drive the evolution of osmoregulatory function in landlocked alewives. We have found that landlocked alewives exhibit lowered activity and expression of the gill ion transporters involved in salt secretion (Na+, K+-ATPase, Na+, K+, 2Cl co-transporter, and cystic fibrosis membrane conductance regulator homolog), which is likely to account for decreases in seawater osmotic balance among landlocked alewives.

Using alewives, we are exploring the transcriptional mechanisms that underlie adaptation to novel salinity regimes. We find that thousands of genes exhibiting salinity-dependent expression have differentiated between alewife life history forms. In particular, genes involved in the gill salt secretion pathway exhibit reduced transcriptional regulation in response to seawater among landlocked alewife populations, while genes involved in gill salt uptake and retention exhibit enhanced freshwater expression. A substantial proportion of the genes involved in osmoregulatory functions show parallel patterns of divergence among independently derived landlocked populations. Modifications to the expression of many well-known effectors of osmotic acclimation may underlie the evolution of osmoregulation upon adaptation to a novel salinity environment.

Transporting alewives to the USGS Conte Anadromous Fish Research Center
Transporting alewives to the USGS Conte Anadromous Fish Research Center in Massachusetts

A recent collaborative project with the Michalak Lab at Virginia Tech has identified repeated selection on an allele of β-thymosin in several independently derived landlocked alewife populations across the United States (Michalak et al 2014 J Exp Zool). β-thymosin is involved in cell volume regulation and is thought to be an important component of osmoregulation in fish. Selection for the “freshwater” β-thymosin allele is correlated with increased mRNA expression among landlocked alewives, suggesting that it is under selection in the transition to freshwater.

Evolution of whole-organism performance

Swimming juvenile alewives. Photo by Kai Webler.
Swimming juvenile alewives in the lab. Photo by Kai Webler

Whole-organism performance can be broken into two integrated components: regulatory performance, which measures homeostatic capabilities, and dynamic performance, which measures physically challenging movements of the body. We use the alewife to examine whether evolutionary changes to regulatory performance (e.g., osmoregulation) can influence the evolution of dynamic performance (e.g., swimming ability). Compared to anadromous alewives, landlocked forms exhibit substantially reduced swimming performance after exposure to either freshwater or seawater, indicating that evolved differences in regulatory performance do not influence dynamic performance in this species. In addition, we have described body shape variation between alewife life history forms and found that landlocked alewives are more fusiform than their robust anadromous ancestor (also see Jones et al 2013 Evo Ecol). Although fusiform shapes should in theory provide a swimming advantage over robust shapes, the opposite is true in alewives. Reductions in swimming performance among landlocked Alewives are likely to be a function of relaxed selection on the capacity to migrate to and from breeding grounds.

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