Origins of endemic stickleback from the Queen Charlotte Islands: mitochondrial and morphological evidence

Deagle, Bruce E.; Reimchen, T. E.; Levin, David B.

doi:10.1139/z96-116

Cited by 50 publications

(87 citation statements)

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“…The lack of correspondence in these cases reveals the slow pace of evolution and major differences in population ecology between water bodies. Stickleback populations from the dystrophic and mesotrophic systems examined are genetically very stable, having evolved over thousands of years in relative isolation (Deagle et al, 1996). In contrast, the Swan Lake population undergoes frequent genetic drift as this small water body becomes periodically anoxic, resulting in the death of resident fish, and marine stickleback populations can readily invade as a result of the ocean's proximity.…”

Section: Discussion Heritable Variation In Opsin Expression Tuned To mentioning

confidence: 99%

Pronounced heritable variation and limited phenotypic plasticity in visual pigments and opsin expression of threespine stickleback photoreceptors

Flamarique

Cheng

Bergstrom

et al. 2012

Journal of Experimental Biology

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SUMMARYVertebrate colour vision is mediated by the differential expression of visual pigment proteins (opsins) in retinal cone photoreceptors. Many species alter opsin expression during life, either as part of development or as a result of changes in habitat. The latter, a result of phenotypic plasticity, appears common among fishes, but its cellular origin and ecological significance are unknown. Here, we used adult threespine stickleback fish from different photic regimes to investigate heritable variability and phenotypic plasticity in opsin expression. Fish from clear waters had double cones that expressed long (LWS) and middle (RH2) wavelength opsins, one per double cone member. In contrast, fish from red light-shifted lakes had double cones that were >95% LWS/LWS pairs. All fish had single cones that predominantly expressed a short wavelength (SWS2) opsin but ultraviolet cones, expressing a SWS1 opsin, were present throughout the retina. Fish from red light-shifted lakes, when transferred to clear waters, had a ~2% increase in RH2/LWS double cones, though double cone density remained constant. Comparison of visual pigment absorbance and light transmission in the environment indicated that the opsin complements of double cones maximized sensitivity to the background light, whereas single cones had visual pigments that were spectrally offset from the dominant background wavelengths. Our results indicate that phenotypic plasticity in opsin expression is minor in sticklebacks and of questionable functional significance. Supplementary material available online at

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Section: Discussion Heritable Variation In Opsin Expression Tuned To mentioning

confidence: 99%

Pronounced heritable variation and limited phenotypic plasticity in visual pigments and opsin expression of threespine stickleback photoreceptors

Flamarique

Cheng

Bergstrom

et al. 2012

Journal of Experimental Biology

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“…In our analysis of population relationships, we incorporated the haplotype profiles of Drizzle and Rouge Lakes reported by O'Reilly et al (1993). These lakes represent one of the lake-stream pairs on Graham Island (Drizzle) and a population apparently fixed for the Marine lineage (Rouge Lake), respectively (Reimchen et al 1985;O'Reilly et al 1993;Deagle et al 1996). Frequency distributions of mtDNA haplotypes among populations were compared using chi-square randomization tests using MONTE of REAP (McElroy et al 1992).…”

Section: Discussionmentioning

confidence: 99%

“…The topology of the tree indicates that there is little association between ecotype (stream-or lake-type) and mitochondrial DNA divergence and strongly supports the hypothesis of multiple origins of lake-stream pairs. For instance, morphologically distinct forms from Misty Lake and its outlet stream clustered together while Misty inlet fish (robust-bodied, mottled coloration, well-developed lateral plates and dorsal and pelvic spines) clustered with fish from Rouge Lake on the Queen Charlotte Islands (which lack lateral plates and have greatly reduced spines; Deagle et al 1996). Of further interest is the observation that neither the stream nor lake forms in Misty Lake cluster with comparable morphotypes from Mayer Lake or, in the case of lake fish, Drizzle Lake (Fig.…”

Section: Mitochondrial Dna Population Phylogenymentioning

confidence: 99%

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PARALLEL EVOLUTION OF LAKE-STREAM PAIRS OF THREESPINE STICKLEBACKS (GASTEROSTEUS) INFERRED FROM MITOCHONDRIAL DNA VARIATION

1997

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Abstract.-Three drainage systems in British Columbia, Canada, contain divergent parapatric lake-stream pairs of threespine sticklebacks (Gasterosteus aculeatus): Drizzle and Mayer Lakes on Graham Island, Queen Charlotte Islands, and Misty Lake on northeastern Vancouver Island. Ecological and morphological differences between members of all three lake-stream pairs are strikingly similar; lake fish are melanistic and slim bodied with smaller mouths and more gill rakers than the mottled-brown and robust-bodied stream sticklebacks. We estimated the level of genetic divergence between lake and stream fish in Misty Lake and tested hypotheses of single versus multiple origins of the pairs by assaying mitochondrial DNA (mtDNA) restriction site variation in samples from the three lake systems. MtDNA analysis revealed the existence of two highly divergent lineages differing by 2.7% in sequence. One lineage predominated in Misty stream fish (73%), whereas the other lineage predominated in Misty Lake samples (96%). Comparable forms (lake or stream) in the different lakes did not cluster together in terms of mtDNA nucleotide divergence, suggesting that the pairs have had independent origins. We concluded that: (1) divergent mtDNA lineages in North Pacific sticklebacks stem from historical isolation in the two major glacial refugia proposed for the North Pacific (Beringia and Cascadia); (2) the stream and lake pair in Misty Lake are distinct gene pools; (3) the divergence between parapatric lake and stream Gasterosteus represents parallel evolution having occurred at least twice in the North Pacific; and (4) different scales of evolutionary divergence exist in North Pacific Gasterosteus, that is, a relatively ancient divergence of mtDNA clades as well as recent (i.e., postglacial) divergence of ecotypes within major clades.

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“…First, lake and stream fish in different systems (Misty, Mayer, Drizzle) have evolved similar sets of traits despite their often varying mtDNA clades (see discussion in Thompson et al 1997). Second, either mtDNA clade can predominate in either lakes or streams in different locations (Deagle et al 1996;Thompson et al 1997;E. B. Taylor, unpubl.…”

Section: Alternative 2: Nonequilibrium Conditions and Historical Originsmentioning

confidence: 99%

Adaptive Divergence and the Balance Between Selection and Gene Flow: Lake and Stream Stickleback in the Misty System

2002

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Abstract. We investigated the interplay between natural selection and gene flow in the adaptive divergence of threespine stickleback (Gasterosteus aculeatus) that reside parapatrically in lakes and streams. Within the Misty Lake system (Vancouver Island, British Columbia), stickleback from the inlet stream (flowing into the lake) have fewer gill rakers and deeper bodies than stickleback from the lake-differences thought to facilitate foraging (benthic macroinvertebrates in the stream vs. zooplankton in the open water of the lake). Common-garden experiments demonstrated that these differences have a genetic basis. Reciprocal transplant enclosure experiments showed that lake and inlet stickleback grow best in their home environments (although differences were subtle and often not significant). Release-recapture experiments in the inlet showed that lake fish are less well-suited than inlet fish for life in the stream (higher mortality or emigration in lake fish). Morphological divergence in the wild and under common rearing was greater between the lake and the inlet than between the lake and the outlet. Genetic divergence (mitochondrial DNA and microsatellites) was greatest between the lake and the upper inlet (1.8 km upstream from the lake), intermediate between the lake and the lower inlet (0.9 km upstream), and least between the lake and the outlet stream (1.2 km downstream). Relative levels of gene flow estimated from genetic data showed the inverse pattern. The negative association between morphological divergence and gene flow is consistent with the expectation that gene flow can constrain adaptation. Estimated absolute levels of gene flow also implied a constraint on adaptation in the outlet but not the inlet. Our results suggest that natural selection promotes the adaptive divergence of lake and stream stickleback, but that the magnitude of divergence can be constrained by gene flow.

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Origins of endemic stickleback from the Queen Charlotte Islands: mitochondrial and morphological evidence

Cited by 50 publications

References 38 publications

Pronounced heritable variation and limited phenotypic plasticity in visual pigments and opsin expression of threespine stickleback photoreceptors

Pronounced heritable variation and limited phenotypic plasticity in visual pigments and opsin expression of threespine stickleback photoreceptors

PARALLEL EVOLUTION OF LAKE-STREAM PAIRS OF THREESPINE STICKLEBACKS (GASTEROSTEUS) INFERRED FROM MITOCHONDRIAL DNA VARIATION

Adaptive Divergence and the Balance Between Selection and Gene Flow: Lake and Stream Stickleback in the Misty System

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