Mechanisms underlying parallel reductions in aerobic capacity in non-migratory threespine stickleback (Gasterosteus aculeatus) populations

Abstract

SUMMARYNon-migratory, stream-resident populations of threespine stickleback, Gasterosteus aculeatus, have a lower maximum oxygen consumption (M O2,max ) than ancestral migratory marine populations. Here, we examined laboratory-bred stream-resident and marine crosses from two locations (West and Bonsall Creeks) to determine which steps in the oxygen transport and utilization cascade evolved in conjunction with, and thus have the potential to contribute to, these differences in M O2,max . We found that West Creek stream-resident fish have larger muscle fibres (not measured in Bonsall fish), Bonsall Creek stream-resident fish have smaller ventricles, and both stream-resident populations have evolved smaller pectoral adductor and abductor muscles. However, many steps of the oxygen cascade did not evolve in stream-resident populations (gill surface area, hematocrit, mean cellular hemoglobin content and the activities of mitochondrial enzymes per gram ventricle and pectoral muscle), arguing against symmorphosis. We also studied F1 hybrids to determine which traits in the oxygen cascade have a genetic architecture similar to that of M O2,max . In West Creek, M O2,max , abductor and adductor size all showed dominance of marine alleles, whereas in Bonsall Creek, M O2,max and ventricle mass showed dominance of stream-resident alleles. We also found genetically based differences among marine populations in hematocrit, ventricle mass, pectoral muscle mass and pectoral muscle pyruvate kinase activity. Overall, reductions in pectoral muscle mass evolved in conjunction with reductions in M O2,max in both stream-resident populations, but the specific steps in the oxygen cascade that have a genetic basis similar to that of M O2,max , and are thus predicted to have the largest impact on M O2,max , differ among populations. Supplementary material available online at

Correlates of prolonged swimming performance in F2 hybrids of migratory and non-migratory threespine stickleback ecotypes

“…The grandparents of the F2 hybrid fish used in this study were collected from wild populations living in Bonsall Creek on Vancouver Island (Dalziel et al, 2012a;Dalziel et al, 2012b) …”

“…We have previously shown that differences in prolonged swimming capacity between wild stream-resident and anadromous marine (hereafter referred to as 'marine') stickleback populations (Schaarschmidt and Jürss, 2003;Tudorache et al, 2007) are genetically based (Dalziel et al, 2012a). In addition, we have found that a number of morphological, physiological and biochemical traits predicted to impact prolonged swimming have evolved in conjunction with differences in performance in stream-resident threespine stickleback populations (Dalziel et al, 2012a;Dalziel et al, 2012b). For example, stream-resident fish from Bonsall Creek (Vancouver Island, BC, Canada) have smaller pectoral fins, a less streamlined body shape, a lower maximal metabolic rate, smaller hearts, and smaller and more glycolytic pectoral muscles than migratory marine sticklebacks (Dalziel et al, 2012a;Dalziel et al, 2012b).…”

“…In addition, we have found that a number of morphological, physiological and biochemical traits predicted to impact prolonged swimming have evolved in conjunction with differences in performance in stream-resident threespine stickleback populations (Dalziel et al, 2012a;Dalziel et al, 2012b). For example, stream-resident fish from Bonsall Creek (Vancouver Island, BC, Canada) have smaller pectoral fins, a less streamlined body shape, a lower maximal metabolic rate, smaller hearts, and smaller and more glycolytic pectoral muscles than migratory marine sticklebacks (Dalziel et al, 2012a;Dalziel et al, 2012b). Any of these traits could, in principle, cause reductions in swimming performance in stream-resident fish.…”

Selection on the morphology–physiology‐performance nexus: Lessons from freshwater stickleback morphs

“…While morphological divergence has been the major thrust of stickleback research over the past decade, cementing the species as an exceptional model in evolutionary ecology (Gibson, 2005), there is mounting evidence of the importance of physiology in its adaptation to freshwater (Dalziel, Ou, & Schulte, 2012; DeFaveri, Shikano, Shimada, Goto, & Merilä, 2011; Di Poi, Bélanger, Amyot, Rogers, & Aubin‐Horth, 2016; Kitano et al., 2010). Thus, it is perhaps not surprising that metabolic rate also appears to be under selection in this system.…”

“…Thus, it is perhaps not surprising that metabolic rate also appears to be under selection in this system. While previous work has documented genetically based differences in metabolism between marine and freshwater populations (Dalziel, Ou et al., 2012; Dalziel, Vines et al., 2012), results were interpreted in the context of relaxed selection pressures in freshwater relative to the marine environment, with selection being inferred on the basis of phenotypic similarity across multiple populations. Conversely, this study is the first to formally test for—and confirm—that metabolic differences between marine and freshwater populations are at least partially due to selection: both standard and active metabolic rates showed signals of divergence consistent with selection acting separately on each, but also potentially simultaneously via correlational selection.…”