Predicting future from past: The genomic basis of recurrent and rapid stickleback evolution

Kingman, Garrett A. Roberts; Vyas, Deven N.; Jones, Felicity C.; Brady, Shannon D.; Chen, Heidi I.; Reid, Kerry; Milhaven, Mark; Bertino, Thomas S.; Aguirre, Windsor E.; Heins, David C.; Hippel, Frank von; Park, Peter J.; Kirch, Melanie; Absher, Devin; Myers, R; Palma, Federica Di; Bell, Michael A.; Kingsley, David M.; Veeramah, Krishna R.

doi:10.1126/sciadv.abg5285

Cited by 69 publications

(80 citation statements)

References 125 publications

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“…To identify novel loci controlling adaptations in threespine stickleback, we measured dorsal spine 1 (DS1), dorsal spine 2 (DS2), and pelvic spine (PS) length on 115 fish previously used for whole-genome sequencing ( 18 ). These major spines vary significantly in size among stickleback populations, including different freshwater populations ( Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Several previous studies have identified genomic sequences that show prominent differentiation between most marine and freshwater stickleback ( 16 – 18 , 50 , 51 ). Having identified multiple alleles at Maser that are associated with contrasting phenotypes among different freshwater populations, we searched stickleback genome sequences for other loci that also show triallelic differentiation among diverse populations from the Pacific Northwest.…”

Section: Resultsmentioning

confidence: 99%

“…The associated genome sequences are available at the Sequence Read Archive (accession no. PRJNA247503) and are more thoroughly described by Marques et al ( 50 ) and Roberts Kingman et al ( 18 ).…”

Section: Methodsmentioning

confidence: 99%

“…All coordinates and alignments are relative to reference genome version gasAcu1-4 ( 18 ). See also https://datadryad.org/stash/dataset/doi:10.5061/dryad.547d7wm6t 10.5061/dryad.547d7wm6t for further resources on this reference version.…”

Section: Methodsmentioning

confidence: 99%

“…A key unanswered question is whether diverse evolutionary outcomes occur by modifying different genes in different environments or by modifying the same genes in different ways. Ancient alleles have been identified at particular loci that allow rapid evolution of common marine-freshwater differences by repeated selection of standing variants that already preexist at low frequencies in marine ancestors ( 14 – 18 ). Repeated fixation of preexisting variants favors the reuse of not only the same gene, but also the same freshwater haplotypes in derived populations that share traits.…”

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confidence: 99%

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Longer or shorter spines: Reciprocal trait evolution in stickleback via triallelic regulatory changes inStanniocalcin2a

Kingman

Lee

Jones

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Vertebrates have repeatedly modified skeletal structures to adapt to their environments. The threespine stickleback is an excellent system for studying skeletal modifications, as different wild populations have either increased or decreased the lengths of their prominent dorsal and pelvic spines in different freshwater environments. Here we identify a regulatory locus that has a major morphological effect on the length of stickleback dorsal and pelvic spines, which we term Maser (major spine enhancer). Maser maps in a closely linked supergene complex that controls multiple armor, feeding, and behavioral traits on chromosome IV. Natural alleles in Maser are differentiated between marine and freshwater sticklebacks; however, alleles found among freshwater populations are also differentiated, with distinct alleles found in short- and long-spined freshwater populations. The distinct freshwater alleles either increase or decrease expression of the bone growth inhibitor gene Stanniocalcin2a in developing spines, providing a simple genetic mechanism for either increasing or decreasing spine lengths in natural populations. Genomic surveys suggest many recurrently differentiated loci in sticklebacks are similarly specialized into three or more distinct alleles, providing multiple ancient standing variants in particular genes that may contribute to a range of phenotypes in different environments.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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Longer or shorter spines: Reciprocal trait evolution in stickleback via triallelic regulatory changes inStanniocalcin2a

Kingman

Lee

Jones

et al. 2021

Proc. Natl. Acad. Sci. U.S.A.

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Gene expression in male and female stickleback from populations with convergent and divergent throat coloration

McKinnon

Newsome

Balakrishnan

2022

Ecology and Evolution

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Understanding of genetic mechanisms underlying variation in sexual dichromatism remains limited, especially for carotenoid‐based colors. We addressed this knowledge gap in a gene expression study with threespine stickleback. We compared male and female throat tissues across five populations, including two in which female red coloration has evolved convergently. We found that the expression of individual genes, gene ontologies, and coexpression networks associated with red female color within a population differed between California and British Columbia populations, suggesting differences in underlying mechanisms. Comparing females from each of these populations to females from populations dominated by dull females, we again found extensive expression differences. For each population, genes and networks associated with female red color showed the same patterns for males only inconsistently. The functional roles of genes showing correlated expression with female color are unclear within populations, whereas genes highlighted through inter‐population comparisons include some previously suggested to function in carotenoid pathways. Among these, the most consistent patterns involved TTC39B (Tetratricopeptide Repeat Domain 39B), which is within a known red coloration QTL in stickleback and implicated in red coloration in other taxa.

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The genetics of adaptation in freshwater Eurasian shad (Alosa)

Sabatino

Pereira

Carneiro

et al. 2022

Ecology and Evolution

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Studying the genetics of phenotypic convergence can yield important insights into adaptive evolution. Here, we conducted a comparative genomic study of four lineages (species and subspecies) of anadromous shad ( Alosa ) that have independently evolved life cycles entirely completed in freshwater. Three naturally diverged ( A . fallax lacustris , A . f . killarnensis , and A . macedonica ), and the fourth ( A . alosa ) was artificially landlocked during the last century. To conduct this analysis, we assembled and annotated a draft of the A . alosa genome and generated whole‐genome sequencing for 16 anadromous and freshwater populations of shad. Widespread evidence for parallel genetic changes in freshwater populations within lineages was found. In freshwater A . alosa , which have only been diverging for tens of generations, this shows that parallel adaptive evolution can rapidly occur. However, parallel genetic changes across lineages were comparatively rare. The degree of genetic parallelism was not strongly related to the number of shared polymorphisms between lineages, thus suggesting that other factors such as divergence among ancestral populations or environmental variation may influence genetic parallelism across these lineages. These overall patterns were exemplified by genetic differentiation involving a paralog of ATPase ‐ α1 that appears to be under selection in just two of the more distantly related lineages studied, A . f . lacustris and A . alosa . Our findings provide insights into the genetic architecture of adaptation and parallel evolution along a continuum of population divergence.

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Predicting future from past: The genomic basis of recurrent and rapid stickleback evolution

Cited by 69 publications

References 125 publications

Longer or shorter spines: Reciprocal trait evolution in stickleback via triallelic regulatory changes inStanniocalcin2a

Longer or shorter spines: Reciprocal trait evolution in stickleback via triallelic regulatory changes inStanniocalcin2a

Gene expression in male and female stickleback from populations with convergent and divergent throat coloration

The genetics of adaptation in freshwater Eurasian shad (Alosa)

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