Mutations of small effect underlie most adaptation to new environments, but beneficial variants with large fitness effects are expected to contribute under certain conditions. Genes and genomic regions having large effects on phenotypic differences between populations are known from numerous taxa, but fitness effect sizes have rarely been estimated. We mapped fitness over a generation in an F2 intercross between a marine and a lake stickleback population introduced to a freshwater pond. A quantitative trait locus map of the number of surviving offspring per F2 female detected a single, large-effect locus near
The Threespine Stickleback is ancestrally a marine fish, but many marine populations breed in fresh water (i.e., are anadromous), facilitating their colonization of isolated freshwater habitats a few years after they form. Repeated adaptation to fresh water during at least 10 My and continuing today has led to Threespine Stickleback becoming a premier system to study rapid adaptation. Anadromous and freshwater stickleback breed in sympatry and may hybridize, resulting in introgression of freshwater-adaptive alleles into anadromous populations, where they are maintained at low frequencies as ancient standing genetic variation. Anadromous stickleback have accumulated hundreds of freshwater-adaptive alleles that are disbursed as few loci per marine individual and provide the basis for adaptation when they colonize fresh water. Recent whole-lake experiments in lakes around Cook Inlet, Alaska have revealed how astonishingly rapid and repeatable this process is, with the frequency of 40% of the identified freshwater-adaptive alleles increasing from negligible (∼1%) in the marine founder to ≥50% within ten generations in fresh water, and freshwater phenotypes evolving accordingly. These high rates of genomic and phenotypic evolution imply very intense directional selection on phenotypes of heterozygotes. Sexual recombination rapidly assembles freshwater-adaptive alleles that originated in different founders into multilocus freshwater haplotypes, and regions important for adaptation to freshwater have suppressed recombination that keeps advantageous alleles linked within large haploblocks. These large haploblocks are also older and appear to have accumulated linked advantageous mutations. The contemporary evolution of Threespine Stickleback has provided broadly applicable insights into the mechanisms that facilitate rapid adaptation.
more » « less- Award ID(s):
- 2135085
- NSF-PAR ID:
- 10370250
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 62
- Issue:
- 2
- ISSN:
- 1540-7063
- Format(s):
- Medium: X Size: p. 388-405
- Size(s):
- ["p. 388-405"]
- Sponsoring Org:
- National Science Foundation
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Ectodysplasin (Eda ), a gene having an ancient freshwater allele causing reduced bony armor and other changes. F2 females homozygous for the freshwater allele had twice the number of surviving offspring as homozygotes for the marine allele, producing a large selection coefficient,s = 0.50 ± 0.09 SE. Correspondingly, the frequency of the freshwater allele increased from 0.50 in F2 mothers to 0.58 in surviving offspring. We compare these results to allele frequency changes at theEda gene in an Alaskan lake population colonized by marine stickleback in the 1980s. The frequency of the freshwaterEda allele rose steadily over multiple generations and reached 95% within 20 y, yielding a similar estimate of selection,s = 0.49 ± 0.05, but a different degree of dominance. These findings are consistent with other studies suggesting strong selection on this gene (and/or linked genes) in fresh water. Selection on ancient genetic variants carried by colonizing ancestors is likely to increase the prevalence of large-effect fitness variants in adaptive evolution. -
ABSTRACT The complete genome sequence of an RNA virus was assembled from RNA sequencing of virus particles purified from threespine stickleback intestine tissue samples. This new virus is most closely related to the Eel picornavirus and can be assigned to the genus Potamipivirus in the family Picornaviridae . Its unique genetic properties are enough to establish a new species, dubbed the Threespine Stickleback picornavirus (TSPV). Due to their broad geographic distribution throughout the Northern Hemisphere and parallel adaptation to freshwater, threespine sticklebacks have become a model in evolutionary ecology. Further analysis using diagnostic PCRs revealed that TSPV is highly prevalent in both anadromous and freshwater populations of threespine sticklebacks, infects almost all fish tissues, and is transmitted vertically to offspring obtained from in vitro fertilization in laboratory settings. Finally, TSPV was found in Sequence Reads Archives of transcriptome of Gasterosteus aculeatus , further demonstrating its wide distribution and unsought prevalence in samples. It is thus necessary to test the impact of TSPV on the biology of threespine sticklebacks, as this widespread virus could interfere with the behavioral, physiological, or immunological studies that employ this fish as a model system. IMPORTANCE The threespine stickleback species complex is an important model system in ecological and evolutionary studies because of the large number of isolated divergent populations that are experimentally tractable. For similar reasons, its coevolution with the cestode parasite Schistocephalus solidus , its interaction with gut microbes, and the evolution of its immune system are of growing interest. Herein we describe the discovery of an RNA virus that infects both freshwater and anadromous populations of sticklebacks. We show that the virus is transmitted vertically in laboratory settings and found it in Sequence Reads Archives, suggesting that experiments using sticklebacks were conducted in the presence of the virus. This discovery can serve as a reminder that the presence of viruses in wild-caught animals is possible, even when animals appear healthy. Regarding threespine sticklebacks, the impact of Threespine Stickleback picornavirus (TSPV) on the fish biology should be investigated further to ensure that it does not interfere with experimental results.more » « less
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Abstract The evolutionary consequences of temporal variation in selection remain hotly debated. We explored these consequences by studying threespine stickleback in a set of bar‐built estuaries along the central California coast. In most years, heavy rains induce water flow strong enough to break through isolating sand bars, connecting streams to the ocean. New sand bars typically re‐form within a few weeks or months, thereby re‐isolating populations within the estuaries. These breaching events cause severe and often extremely rapid changes in abiotic and biotic conditions, including shifts in predator abundance. We investigated whether this strong temporal environmental variation can maintain within‐population variation while eroding adaptive divergence among populations that would be caused by spatial variation in selection. We used neutral genetic markers to explore population structure and then analysed how stickleback armor traits, the associated genes
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Abstract Evidence that organisms evolve rapidly enough to alter ecological dynamics necessitates investigation of the reciprocal links between ecology and evolution. Data that link genotype to phenotype to ecology are needed to understand both the process and ecological consequences of rapid evolution. Here, we quantified the suite of elements in individuals (i.e., ionome) and differences in the fluxes of key nutrients across populations of threespine stickleback. We find that allelic variation associated with freshwater adaptation that controls bony plating is associated with changes in the ionome and nutrient recycling. More broadly, we find that adaptation of marine stickleback to freshwater conditions shifts the ionomes of natural populations and populations raised in common gardens. In both cases ionomic divergence between populations was primarily driven by differences in trace elements rather than elements typically associated with bone. These findings demonstrate the utility of ecological stoichiometry and the importance of ionome‐wide data in understanding eco‐evolutionary dynamics.
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