Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer

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Author(s): , M. E. Marks, F. C. Jones, G. Villarreal, M. D. Shapiro, S. D. Brady, A. M. Southwick, D. M. Absher, J. Grimwood, J. Schmutz, R. M. Myers, D. Petrov, B. Jonsson, D. Schluter, M. A. Bell, D. M. Kingsley

Publication date Created: January 14 2010

Publication date (Electronic): December 10 2009

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The molecular mechanisms underlying major phenotypic changes that have evolved repeatedly in nature are generally unknown. Pelvic loss in different natural populations of threespine stickleback fish has occurred through regulatory mutations deleting a tissue-specific enhancer of the Pituitary homeobox transcription factor 1 (Pitx1) gene. The high prevalence of deletion mutations at Pitx1 may be influenced by inherent structural features of the locus. Although Pitx1 null mutations are lethal in laboratory animals, Pitx1 regulatory mutations show molecular signatures of positive selection in pelvic-reduced populations. These studies illustrate how major expression and morphological changes can arise from single mutational leaps in natural populations, producing new adaptive alleles via recurrent regulatory alterations in a key developmental control gene.

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Molecular signatures of natural selection.

There is an increasing interest in detecting genes, or genomic regions, that have been targeted by natural selection. The interest stems from a basic desire to learn more about evolutionary processes in humans and other organisms, and from the realization that inferences regarding selection may provide important functional information. This review provides a nonmathematical description of the issues involved in detecting selection from DNA sequences and SNP data and is intended for readers who are not familiar with population genetic theory. Particular attention is placed on issues relating to the analysis of large-scale genomic data sets.

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Widespread parallel evolution in sticklebacks by repeated fixation of Ectodysplasin alleles.

Major phenotypic changes evolve in parallel in nature by molecular mechanisms that are largely unknown. Here, we use positional cloning methods to identify the major chromosome locus controlling armor plate patterning in wild threespine sticklebacks. Mapping, sequencing, and transgenic studies show that the Ectodysplasin (EDA) signaling pathway plays a key role in evolutionary change in natural populations and that parallel evolution of stickleback low-plated phenotypes at most freshwater locations around the world has occurred by repeated selection of Eda alleles derived from an ancestral low-plated haplotype that first appeared more than two million years ago. Members of this clade of low-plated alleles are present at low frequencies in marine fish, which suggests that standing genetic variation can provide a molecular basis for rapid, parallel evolution of dramatic phenotypic change in nature.

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The genetic theory of adaptation: a brief history.

Theoretical studies of adaptation have exploded over the past decade. This work has been inspired by recent, surprising findings in the experimental study of adaptation. For example, morphological evolution sometimes involves a modest number of genetic changes, with some individual changes having a large effect on the phenotype or fitness. Here I survey the history of adaptation theory, focusing on the rise and fall of various views over the past century and the reasons for the slow development of a mature theory of adaptation. I also discuss the challenges that face contemporary theories of adaptation.

Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer

Publication Type Manuscript
School or College College of Science
Department Biology
Creator Shapiro, Michael D.
Other Author Chan, Yingguang Frank; Marks, Melissa E.; Jones, Felicity C.; Villarreal Jr., Guadalupe; Brady, Shannon D.; Southwick, Audrey M.; Absher, Devin M.; Grimwood, Jane; Schmutz, Jeremy; Myers, Richard M.; Petrov, Dmitri; Jónsson, Bjarni; Schluter, Dolph; Bell, Michael A.; Kingsley, David M.
Title Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer
Date 2010-01-14
Description The molecular mechanisms underlying major phenotypic changes that have evolved repeatedly in nature are generally unknown. Pelvic loss in different natural populations of threespine stickleback fish has occurred by regulatory mutations deleting a tissue-specific enhancer of the Pituitary homeobox transcription factor 1 (Pitx1) gene. The high prevalence of deletion mutations at Pitx1 may be influenced by inherent structural features of the locus. Although Pitx1 null mutations are lethal in laboratory animals, Pitx1 regulatory mutations show molecular signatures of positive selection in pelvic-reduced populations. These studies illustrate how major expression and morphological changes can arise by single mutational leaps in natural populations, producing new adaptive alleles via recurrent regulatory alterations in a key developmental control gene.
Type Text
Publisher American Association for the Advancement of Science (AAAS)
Journal Title Science
Volume 327
Issue 5963
First Page 302
Last Page 305
DOI 10.1126/science.1182213
citatation_issn 0036-8075
Subject Adaptive evolution; Pelvic reduction; Pituitary homeobox transcription factor 1; Pitx1; Gasterosteus aculeatus
Subject LCSH Sticklebacks -- Evolution; Threespine stickleback -- Evolution
Language eng
Bibliographic Citation Chan, Y. F., Marks, M. E., Jones, F. C., Villarreal, G., Shapiro, M. D., Brady, S. D., Southwick, A. M., Absher, D. M., Grimwood, J., Schmutz, J., Myers, R. M., Petrov, D., Jónsson, B., Schluter, D., Bell, M. A., & Kingsley, D. M. (2010). Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science, 327, 302-5.
Rights Management (c)American Association for the Advancement of Science (AAAS) //dx.doi.org/10.1126/science.1182213
Format Medium application/pdf
Format Extent 894,818 bytes
Identifier ir-main,11962
ARK ark:/87278/s68d0dkq
Setname ir_uspace
Date Created 2012-06-13
Date Modified 2021-05-06
ID 704363
Reference URL //collections.lib.utah.edu/ark:/87278/s68d0dkq

What is mutated in Pitx1 in freshwater sticklebacks?

Mike Shapiro, PhD, a postdoctoral scholar and co-first author, found that a gene located at that region is the stickleback version of a gene in mice called Pitx1 that, when mutated, causes mice to have greatly reduced hind limbs. These mice often have asymmetric limb and pelvic reductions, much like the sticklebacks.

Why do you think stickleback fish with a Pitx1 mutation are able to survive but not the mice?

c) Why do you think stickleback fish with a Pitx1 mutation are able to survive but not the mice? By knocking out the protein-coding region of the Pitx1 gene in mice, the gene can no longer be expressed in any cells of the organism. The Pitx1 protein is critical for the normal development of the pituitary gland and jaw.

What happened to the Pitx1 pelvic switch in freshwater fish?

A mutation in the pelvic switch shuts off the Pitx1 gene in the pelvis. This prevents the development of pelvic spines. 2. According to the film, what is the selective pressure that led to freshwater stickleback fish losing their pelvic spines?

What did researchers discover about the genetic mutation causing the loss of pelvic spines?

What did researchers discover about the genetic mutation causing the loss of pelvic spines? It is found in the coding region of the Pitx1 gene. It results in a protein that is no longer functional. It is always found in one of the regulatory "switches" near the coding region of the Pitx1 gene.

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