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Variation Among Lake Chub (Cyprinidae: Couesius Plumbeus) Populations*

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Variation Among Lake Chub (Cyprinidae: Couesius Plumbeus) Populations* 000 Thermal Physiology of Warm-Spring Colonists: Variation among Lake Chub (Cyprinidae: Couesius plumbeus) Populations* Charles-A. Darveau1,† ature population, while it increased with decreasing acclimation Eric B. Taylor1,2 temperature in both variable thermal habitat populations. Our Patricia M. Schulte1 study suggests that interpopulation variation in thermal physi- 1Department of Zoology, University of British Columbia, ology is associated with habitat thermal variability. 6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Canada; 2Biodiversity Research Centre and Beaty Biodiversity Museum, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia V6T 1Z4, Introduction Canada Temperature has pervasive effects on biological systems and Accepted 10/9/2011; Electronically Published 3/20/2012 thus may be important in establishing the distribution and abundance patterns of ectotherms (Bullock 1955; Hochachka and Somero 2002). The thermal range that a species can inhabit may vary from narrow (in stenotherms) to wide (in eurytherms; ABSTRACT reviewed in Somero et al. 1996), and the position and breadth In northern Canada, lake chub (Cyprinidae: Couesius plumbeus) of that range can be modified by acclimation (Cossins and have colonized a variety of thermal springs that differ substan- Bowler 1987). The capacity to make the biochemical and phys- tially from the ancestral environment in both mean temperature iological adjustments associated with acclimation, however, var- and thermal variation. To examine whether this environmental ies substantially among species (Cossins and Bowler 1987). Al- change is associated with differences in physiological traits, we though there has been substantial debate in the evolutionary compared the thermal breadth, capacity for acclimation of ther- physiology literature with respect to the adaptive value of ac- mal tolerance, and metabolic enzymes in populations of lake climation (e.g., Wilson and Franklin 2002; Woods and Harrison chub from three habitats: a warm but variable hot spring, a 2002), it is clear that the capacity for beneficial acclimation, a thermally constant warm spring, and a seasonally variable tem- form of adaptive phenotypic plasticity, would be expected to perate lake. Thermal breadth was generally lowest in fish from evolve only under certain circumstances (Padilla and Adolph the constant environment, and this difference was statistically 1996; for a review, see Piersma and van Gils 2010). These the- significant in fish acclimated at 10Њ and 25ЊC. Critical thermal oretical considerations suggest that plasticity will evolve only maximum (CTmax) increased with increasing acclimation tem- when the environment varies in a predictable way and on an perature in all populations. CTmax was similar among populations appropriate timescale with respect to the life span of the or- when acclimated at high temperatures but greater in the variable- ganism and the speed of the plastic responses and is likely to spring population acclimated to low temperature (10ЊC). Critical be lost in constant environments when positive selection for thermal minimum was also dependent on acclimation temper- plasticity is relaxed—a process that may occur rapidly if the ature in all populations but differed among populations such costs of maintaining plasticity are high (Lahti et al. 2009). that fish from the stable-spring habitat were not as tolerant to Acclimatory responses are common in ectotherms inhabiting cold temperature when acclimated to 25ЊC. Temperate- and var- temperate environments that are characterized by predictable iable-spring populations showed an increase in mitochondrial seasonal variation in temperature. At the whole-animal level, enzyme activities (citrate synthase and cytochrome c oxidase) compensatory changes in locomotor performance and thermal with decreasing acclimation temperature, but this response was tolerance are often observed (Beitinger et al. 2000; Johnston absent in the stable-temperature population. Protein content did and Temple 2002). For example, Beitinger et al. (2000) reviewed not change with acclimation temperature in the stable-temper- variation in upper and lower limits among fish species (mea- sured as critical thermal maxima and minima, the temperature at which fish are no longer able to maintain equilibrium) and * This paper was submitted in response to a call for papers for a Focused Issue on “Intraspecific Variation in Physiology and Behavior.” demonstrated that this trait shows a high degree of plasticity † Corresponding author. Present address: Department of Biology, University of and that the extent of the plasticity tends to be greatest in Ottawa, 30 Marie Curie, Ottawa, Ontario K1N 6N5, Canada; e-mail: cdarveau@ temperate-zone fishes. At the suborganismal level, ectotherms uottawa.ca. often respond to thermal acclimation by modifying aspects of Physiological and Biochemical Zoology 85(6):000–000. 2012. ᭧ 2012 by The cellular metabolism, including mitochondrial and membrane University of Chicago. All rights reserved. 1522-2152/2012/8506-1084$15.00. properties (reviewed in Guderley 2004). For example, a typical DOI: 10.1086/665539 compensatory response to cold acclimation consists of an in- 000 C.-A. Darveau, E. B. Taylor, and P. M. Schulte crease in mitochondrial abundance, as indicated by the activity transfer licence 10409 a-e). Populations living in contrasting of mitochondrial enzymes citrate synthase and cytochrome c thermal habitats were sampled, including two thermal-spring oxidase, and has been documented in fish (reviewed in Gud- populations: Liard Hot Spring (59Њ2542.69, Ϫ126Њ518.32) erley 2004), marine invertebrates (Lurman et al. 2010), am- and Atlin Warm Spring (59Њ2413.98, Ϫ133Њ3431.21) popu- phibians (Berner and Puckett 2010), and reptiles (Seebacher lations. Various habitats (creeks, rivers, ponds, and lakes) neigh- 2005). Thus, metabolic compensations appear to be a stereo- boring the springs were sampled using a seine net and minnow typical response of eurythermic animals that remain active in traps, but no lake chub were captured during our sampling low-temperature conditions. effort. As a result, we utilized fish from Green Lake The colonization of thermal springs by temperate-zone fishes (51Њ2234.60, Ϫ121Њ1546.97), which (although distant from provides an interesting model system in which to explore the the two spring populations) is likely representative of the pu- effects of relaxation of selection on the capacity for thermal tative ancestral thermal habitat. In fact, all study populations acclimation. The lake chub (Couesius plumbeus)isasmall- belong to a common “western” mitochondrial DNA lineage bodied member of the Cyprinidae (carps and minnows) that (E. B. Taylor, unpublished data), and the limited geographic is native to a vast area of North America. The lake chub is distribution of contemporary lake chub populations in the Co- native to lakes and streams from the Atlantic basin in Canada lumbia River (part of the Pacific Refuge) and the Yukon River and the United States, west to the Rocky Mountains in the (the heart of the Bering Refuge) suggests that all lake chub in United States, north and west to the Pacific basin in British western North America probably had a common origin from Columbia (BC), and north and east to the Arctic basin in a Great Plains refuge (cf. McPhail and Lindsey 1970). All pop- northwestern Canada and Alaska and to Labrador (Lee et al. ulations were sampled during the months of July and August 1980). The lake chub achieved this large range from postglacial 2005, using minnow traps or a dip net. Live fish (80 per pop- range expansion following retreat of the Wisconsinan glaciers ulation) were transported in aerated plastic bags filled with the beginning about 10,000 years ago and in the process of degla- respective habitat water at a density of approximately 1 fish/L ciation have colonized a small number of thermal springs in and maintained on ice in a Styrofoam box placed in a cardboard northwestern BC (McPhail 2007). The vast majority of lake box for transport. Water temperature ranged from 3Њ to 7ЊC chub populations, however, live in lakes and streams that ex- during transport, which ranged from 8 h for the Green Lake perience an environment with strong seasonal variation in tem- population to 24 h for the spring populations. In addition, for perature, with water temperatures ranging from approximately spring populations, 10 individuals were frozen immediately in 4ЊC in the winter to the mid-20s (ЊC) in the summer. In con- liquid nitrogen after capture and transported in a cryogenic trast, thermal-spring colonists experience much more stable shipper. Water temperatures in each habitat at the time of sam- thermal conditions. For instance, Atlin Warm Spring (north- pling were recorded using a digital temperature probe (Quartz western BC) maintains a relatively constant water temperature Digi-Thermo, Fisher Scientific). of 23Њ–25ЊC year-round despite a yearly average daily air tem- perature of 0.5ЊC, average daily temperatures that range be- tween Ϫ15Њ and Ϫ5ЊC from December to March, and daily air Fish Holding Conditions and Temperature Acclimation temperatures that range between 6Њ and 13ЊCfromMayto Experiment September (Environment Canada 2011). We hypothesized that Upon arrival at the University of British Columbia (UBC), fish thermal-spring populations, which experience relatively con- were transferred to four 100-L aquaria where the initial water stant temperatures, would
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