Skip Navigation


Journal of Heredity Advance Access originally published online on August 9, 2007
Journal of Heredity 2007 98(6):581-586; doi:10.1093/jhered/esm066
This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
98/6/581    most recent
esm066v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (9)
Right arrowRequest Permissions
Google Scholar
Right arrow Articles by Coyle, S. M.
Right arrow Articles by Peichel, C. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Coyle, S. M.
Right arrow Articles by Peichel, C. L.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

© The American Genetic Association. 2007. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org.

Parallel Evolution of Pitx1 Underlies Pelvic Reduction in Scottish Threespine Stickleback (Gasterosteus aculeatus)

Susan M. Coyle, Felicity A. Huntingford, and Catherine L. Peichel

From the Division of Evolutionary and Environmental Biology, Graham Kerr Building, University of Glasgow, Scotland, G12 8QQ, UK (Coyle and Huntingford); and the Division of Human Biology, 1100 Fairview Avenue North, Fred Hutchinson Cancer Research Center, Seattle, WA 98109-1024 (Peichel)

Address correspondence to C. L. Peichel at the address above, or e-mail: cpeichel{at}fhcrc.org.

Little is known about the genetic and molecular mechanisms that underlie adaptive phenotypic variation in natural populations or whether similar genetic and molecular mechanisms are utilized when similar adaptive phenotypes arise in independent populations. The threespine stickleback (Gasterosteus aculeatus) is a good model system to investigate these questions because these fish display a large amount of adaptive phenotypic variation, and similar adaptive phenotypes have arisen in multiple, independent stickleback populations. A particularly striking pattern of parallel evolution in sticklebacks is reduction of skeletal armor, which has occurred in numerous freshwater locations around the world. New genetic and genomic tools for the threespine stickleback have made it possible to identify genes that underlie loss of different elements of the skeletal armor. Previous work has shown that regulatory mutations at the Pitx1 locus are likely responsible for loss of the pelvic structures in independent stickleback populations from North America and Iceland. Here we show that the Pitx1 locus is also likely to underlie pelvic reduction in a Scottish population of threespine stickleback, which has apparently evolved pelvic reduction under a different selection regime than the North American populations.

Although the selective forces that contribute to adaptive phenotypic variation are beginning to be understood, very little is known about the genetic changes on which selection acts during phenotypic evolution (Orr 2005). The threespine stickleback (Gasterosteus aculeatus) is an excellent model system in which to integrate ecological and genetic studies to gain a greater understanding of the process of phenotypic evolution (Foster and Baker 2004; Kingsley et al. 2004; Gibson 2005; Kingsley and Peichel 2007). This small teleost fish displays such great phenotypic variation that different forms were originally classified as more than 40 different species, with some of the most obvious phenotypic changes in stickleback populations occurring in skeletal armor. In most locations, these fish are encased in bony armor that consists of lateral plates, dorsal spines, and 2 pelvic spines supported by a pelvic girdle. However, armor reduction has occurred in freshwater locations that have only existed since the retreat of the glaciers less than 20 000 years ago. In particular, pelvic reduction has occurred in a small number of independent locations ranging from the northwest coast of Scotland to Iceland to several sites along the Pacific coast of North America (Bell 1974, 1987; Moodie and Reimchen 1976; Campbell 1979; Bell et al. 1993; Shapiro et al. 2004). The evolution of armor reduction is associated with specific predation regimes and low calcium levels in North American populations (Reimchen 1980; Bell et al. 1993) but is solely associated with low calcium levels in Scottish populations (Giles 1983).

The development of genetic and genomic tools for threespine stickleback has made it possible to identify the genetic and molecular basis of phenotypic variation in natural populations of this species (Peichel 2005; Kingsley and Peichel 2007). Genome-wide linkage mapping carried out using Canadian pelvic-reduced populations identified the Pitx1 gene as a candidate locus of large effect for pelvic size (Shapiro et al. 2004). Genetic crosses suggest that the same locus also underlies pelvic reduction in Icelandic and Alaskan threespine stickleback populations (Cresko et al. 2004; Shapiro et al. 2004) as well as pelvic reduction in a closely related species, the ninespine stickleback (Shapiro et al. 2006). In Canadian and Scottish pelvic-reduced populations, gene expression studies have demonstrated that Pitx1 is not expressed in the developing pelvic region (Cole et al. 2003; Shapiro et al. 2004). However, mapping studies had not been carried out in the Scottish population, so it was unknown whether the loss of Pitx1 expression in this population is genetically linked to the Pitx1 locus or results from a mutation in an unlinked gene that regulates Pitx1 expression. Here we show that the pelvic reduction phenotype is tightly linked to the Pitx1 locus in a Scottish population. Although our data do not rule out the possibility that the loss of Pitx1 expression in this Scottish population results from changes in a closely linked gene that regulates Pitx1 expression, this result provides evidence that changes at or near the Pitx1 locus have occurred in multiple, independent stickleback populations with pelvic reduction.


   Materials and Methods
Top
 Materials and Methods
Results and Discussion
 Funding
 Supplementary Material
 References
 
Fish
Sticklebacks from the River Kelvin (Glasgow, Scotland) and Loch Fada (North Uist, Scotland) were caught in February 2003 and transported in aerated 25-gallon buckets to the Glasgow University Field Station (SCENE), Loch Lomondside. Fish from a single population were kept together in 1.3 x 1.3 m, 500-l flow-through indoor tanks at a maximum density of 40 fish per tank. Several large plastic plants were placed in each tank as a refuge for fish to hide in. Fish were fed frozen and live bloodworm (Chironomous spp.) and frozen water fleas (Daphnia spp.) ad libitum and maintained on an ambient photoperiod at ambient loch water temperature (6 ± 2 °C).

Crosses
For genetic mapping, 1 Loch Fada female that had no pelvic spines or pelvic girdle structures (pelvic score = 0; Bell et al. 1993) was crossed with 1 River Kelvin male that had 2 pelvic spines and complete pelvic girdle structures (pelvic score = 8) to produce 40 F1 offspring. Eight of these F1 fish were intercrossed, resulting in 177 F2 progeny from 4 F2 families (Table 1). The F1 parents of all families had complete pelvic girdles and 2 pelvic spines (pelvic score = 8), except for the Family 4 F1 father, which had a complete pelvic girdle but was missing the right pelvic spine (pelvic score = 7).


View this table:
[in this window]
[in a new window]

  		Table 1. Pelvic spine number in F2 cross fish

 
Males in breeding condition were moved to sandy bottomed breeding tanks (45 x 27 x 15 cm) with nesting material. After nest construction, a gravid female was placed in the tank and the pair was left to breed naturally. After spawning, the female was removed and the fertilized eggs placed in an incubator and artificially oxygenated at 16 °C. Males rebuilt a nest within 1–3 days, and a gravid female was returned to the tank to breed again. Fry were fed Liquifry No1 (INTERPET) for 1 week after hatching and then maintained on a mixture of enriched AF high-grade Artemia (INVE AQUACULTURE nv) and chopped bloodworm. At 8 weeks, fry were moved to small holding tanks (25 x 20 x 45 cm) and kept in family groups of 10–15 fish.

Phenotypic Analysis
Parental and F1 adults and F2 fish at 24 weeks after hatching were killed with an overdose of anesthetic (benzocaine). Fins were clipped for DNA extraction, and the bodies were preserved in 100% ethanol. The number of pelvic spines was counted, and measurements of standard length (tip of snout to end of caudal peduncle), pelvic spine lengths (tip to anterior edge of spine), and ventral pelvic girdle length (between spines to posterior tip of girdle) were made with calipers to the nearest 0.1 mm. Asymmetry was calculated as the ratio of the length of the left pelvic spine to the combined length of the left and right pelvic spines, such that a value of 0.5 indicates perfect symmetry, a value of 0.0 indicates the loss of the left pelvic spine, and a value of 1.0 indicates loss of the right pelvic spine.

Genetic Analysis
Six microsatellite markers (Stn76, Stn257, Stn80, Stn82, Stn336, Stn342) previously mapped to linkage group 7 (LG7) were used for genotyping (Shapiro et al. 2004). These markers are found in the G. aculeatus sequence assembly BROAD S1 (http://www.ensembl.org/Gasterosteus_aculeatus/index.html) at approximately 5.22 Mb (Stn76), 25.10 Mb (Stn257), 26.40 Mb (Stn80), and 26.66 Mb (Stn82) on LG7, and on scaffold 76 (Stn336, Stn342), which has not been assigned to a LG in the sequence assembly. These markers were used to genotype 177 F2 progeny as well as the grandparents and F1 parents, using previously described polymerase chain reaction (PCR) conditions (Peichel et al. 2001). However, the DNAs of 2 fish were not included in the genetic analysis (Loch Fada grandmother and Family 2 F1 mother). PCRs were analyzed on an ABI 3100 (Applied Biosystems, Foster City, CA). Two people independently determined genotypes by manually calling the allele sizes and segregation patterns, which were visualized with ABI GeneMapper 3.7 (Applied Biosystems). A map of LG7 was generated in JoinMap 3.0 (Van Ooijen and Voorips 2001) using the default settings, and interval mapping of 5 pelvic traits was performed in MapQTL 4.0 (Van Ooijen et al. 2002) using default settings. Likelihood of odds (LOD) significance thresholds were determined for each trait by permutation tests in MapQTL 4.0 using a chromosome-wide significance threshold of {alpha} = 0.01 for n = 1000 permutations. Because only 1 chromosome was genotyped and tested, the chromosome-wide and genome-wide LOD significance thresholds are equivalent.


   Results and Discussion
Top
 Materials and Methods
 Results and Discussion
Funding
 Supplementary Material
 References
 
We crossed a female completely lacking pelvic spines and pelvic girdle structures from an armor-reduced Scottish population (Loch Fada) known to lack pelvic Pitx1 expression (Cole et al. 2003) to a male with a complete pelvic complex from a robustly armored Scottish population (River Kelvin). From this cross we generated 40 F1 progeny, which all had complete pelvic structures, except for 3 fish that had complete pelvic girdles, but showed loss of the right pelvic spine. Four pairs of full-sib F1 hybrid fish were intercrossed to generate 4 F2 families, producing a total of 177 F2 progeny (Figure 1 and Table 1). In the F2 progeny, there was an approximate 3:1 ratio of progeny with complete pelvic girdles and either 2 or 1 pelvic spines to progeny with no pelvic structures (Figure 1; {chi}2 = 0.996, P = 0.318, degrees of freedom = 1). These data suggested that there might be a major locus responsible for loss of the pelvic complex in this Scottish population, as seen in Canadian and Alaskan populations (Cresko et al. 2004; Shapiro et al. 2004).


Figure 1
View larger version (26K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		Figure 1. Intercross for genetic mapping of pelvic reduction. Line drawings of representative fish, with pelvic structures highlighted in red are shown for the parental, F1, and F2 generation. Both lateral and dorsal views of the parental fish are shown to highlight the complete absence of pelvic structures (girdle and spines) in the Loch Fada mother. The ascending branch of the pelvic girdle can be seen in the lateral view of the River Kelvin father, and the ventral pelvic girdle and 2 pelvic spines can be seen in the ventral view of the River Kelvin male. Only ventral views of representative F2 fish are shown to emphasize the different pelvic spine classes. Genotypes at the Pitx1 microsatellites (Stn 336/Stn 342) are indicated in parenthesis.

 
To determine whether Pitx1 is genetically linked to the major pelvic reduction locus in the Loch Fada population, we genotyped F2 fish with 6 informative microsatellite markers from stickleback LG7, including 2 markers in the Pitx1 gene, to which the major pelvic locus has been mapped in other populations (Cresko et al. 2004; Shapiro et al. 2004). Of the 50 F2 fish that had complete loss of pelvic structures, all inherited 2 Fada alleles at the Pitx1 markers (Figure 1). Interval mapping showed that the Pitx1 locus explains between 85.1% and 96.6% of the variance in pelvic spine length and number, as well as pelvic girdle length, with LOD scores between 72.0 and 129.3 (Figure 2 and Table 2). These mapping data, together with the previous evidence for lack of pelvic Pitx1 expression in the Fada population (Cole et al. 2003), provide strong evidence that mutations at the Pitx1 locus or at a tightly linked gene that regulates Pitx1 expression, rather than an unlinked gene that regulates Pitx1 expression, are largely responsible for pelvic reduction in this Scottish population.


View this table:
[in this window]
[in a new window]

  		Table 2. Effect of Pitx1 on pelvic phenotypes

 


Figure 2
View larger version (16K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		Figure 2. Interval mapping of pelvic traits on LG7. LOD scores are plotted as a function of the position in cM of markers: Stn76 (0.0 cM), Stn257 (31.5 cM), Stn80 (42.2 cM), Stn82 (47.6 cM), Stn336/Pitx1 (61.8 cM), and Stn342/Pitx1 (61.8 cM), which are indicated by points along the curve.

 
The high percentage of phenotypic variance explained by the Pitx1 locus in these crosses suggests that modifier loci with detectable effects on pelvic phenotype are not segregating in the Loch Fada population. Furthermore, the Pitx1 locus explains similar levels of phenotypic variance across all 4 F2 families, suggesting that we are not detecting within-population genetic variation for pelvic reduction (Supplementary Table 1). These results differ from mapping studies in a Canadian pelvic-reduced population, where the Pitx1 locus explained 46.8% and 65.3% of the variance in pelvic girdle length and pelvic spine length, respectively, and 4 modifier loci of smaller effect were genetically mapped (Shapiro et al. 2004). Modifier loci with minor effects on pelvic phenotypes are also segregating in Alaskan populations (Cresko et al. 2004). Consistent with our findings for pelvic reduction in the Loch Fada population, modifier loci for armor plate reduction were identified in a Canadian but not in a Californian threespine stickleback population (Colosimo et al. 2004), suggesting that the presence of modifiers of smaller effect may vary between stickleback populations.

Interestingly, 3 of the F1 fish and 4 of the F2 fish had complete pelvic structures, except for loss of the right pelvic spine, whereas a single F2 fish had complete pelvic structures except for loss of the left pelvic spine (Figure 1 and Table 1). This left-biased asymmetry is consistent with previous results in both natural populations (Bell 1974, 1987; Moodie and Reimchen 1976; Bell et al. 1985, 2007) and laboratory crosses (Cresko et al. 2004; Shapiro et al. 2004). This observation is also consistent with the fact that the loss of Pitx1 can be partially compensated by Pitx2, which is preferentially expressed on the left side of the body (Marcil et al. 2003). Of the 5 F2 fish with a single pelvic spine, 2 were homozygous for the Fada alleles at the Pitx1 markers, whereas 3 (including the fish that had lost the left pelvic spine) were heterozygous at the Pitx1 markers (Figure 1). Interval mapping revealed that the Pitx1 locus explains 38% of the asymmetry in pelvic spine length, with a significant LOD score of 13.2 (Figure 2 and Table 2), consistent with previous results (Shapiro et al. 2004).

We thus conclude that pelvic reduction in the Scottish Loch Fada population, which has likely evolved as a result of selection under low calcium levels rather than lack of piscivorous fish predators (Giles 1983), represents a case of parallel evolution at or near the Pitx1 locus. Recent genetic studies in a number of taxa have uncovered other examples of parallel evolution involving the same locus. For example, the yellow gene controls changes in wing pigmentation in different Drosophila species (Gompel and Carroll 2003; Gompel et al. 2005; Prud'homme et al. 2006), the shavenbaby/ovo gene is responsible for changes in hair patterns in Drosophila species (Sucena et al. 2003), coding mutations in the Mc1r gene result in melanism in many vertebrate lineages (Theron et al. 2001; Eizirik et al. 2003; Nachman et al. 2003; Mundy et al. 2004; Rosenblum et al. 2004; Hoekstra et al. 2006; Römpler et al. 2006), and the Oca2 gene is responsible for albinism in fish and mammals (Protas et al. 2006). The recurrent use of a small set of genes during morphological evolution suggests that genetic and/or developmental bias may play an important role in adaptation. Additional studies to identify the molecular changes that give rise to loss of pelvic structures in Canadian, Alaskan, Icelandic, and Scottish populations will allow us to determine whether parallel evolution of pelvic reduction results from standing genetic variation in the ancestral marine population as found for loss of bony lateral plates (Colosimo et al. 2005) or from independent mutations, implicating genetic and/or developmental bias as a key factor in the evolution of pelvic reduction in stickleback.


   Funding
Top
 Materials and Methods
 Results and Discussion
 Funding
Supplementary Material
 References
 
Burroughs Wellcome Fund Career Award in the Biomedical Sciences (to C.L.P.). The Natural Environmental Research Council (NERC), Scottish Natural Heritage and Glasgow Natural History Society (to S.M.C. and F.A.H.).


   Supplementary Material
Top
 Materials and Methods
 Results and Discussion
 Funding
 Supplementary Material
References
 
Supplementary material can be found at http://www.jhered.oxfordjournals.org/.


   Acknowledgments
 
We would like to thank Gill Andrew, Diane Baum, and Dan Thornham and the staff at SCENE field station for assistance as well as Mike Shapiro and Anna Greenwood for helpful comments on the manuscript.


   Footnotes
 
Corresponding Editor: William Modi

Received September 1, 2006
Accepted May 30, 2007


   References
Top
 Materials and Methods
 Results and Discussion
 Funding
 Supplementary Material
 References
 

    Bell MA. Reduction and loss of the pelvic girdle in Gasterosteus (Pisces): a case of parallel evolution. Nat Hist Mus Los Angel Contrib Sci. (1974) 257:1–36.

    Bell MA. Interacting evolutionary constraints in pelvic reduction of threespine sticklebacks, Gasterosteus aculeatus (Pisces, Gasterosteidae). Biol J Linn Soc. (1987) 31:347–382.[Web of Science]

    Bell MA, Francis RC, Havens AC. Pelvic reduction and its directional asymmetry in threespine sticklebacks from the Cook Inlet region in Alaska. Copeia (1985) 1985:437–444.[CrossRef]

    Bell MA, Khalef V, Travis MP. Directional asymmetry of pelvic vestiges in threespine stickleback. J Exp Zoolog Mol Dev Evol. (2007) 308B:189–199.

    Bell MA, Orti G, Walker JA, Koenings JP. Evolution of pelvic reduction in threespine stickleback fish—a test of competing hypothesis. Evolution (1993) 47:906–914.[CrossRef][Web of Science]

    Campbell RN. Sticklebacks (Gasterosteus aculeatus L. and Pungitius pungitius L.) in the Outer Hebrides, Scotland. Heb Nat (1979) 3:8–15.

    Cole NJ, Tanaka M, Prescott A, Tickle C. Expression of limb initiation genes and clues to the morphological diversification of threespine stickleback. Curr Biol. (2003) 13:R951–R952.[CrossRef][Web of Science][Medline]

    Colosimo PF, Hosemann KE, Balabhadra S, Villareal G, Dickson M, Grimwood J, Schmutz J, Myers RM, Schluter D, Kingsley DM. Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science (2005) 307:1928–1933.[Abstract/Free Full Text]

    Colosimo PF, Peichel CL, Nereng K, Blackman BK, Shapiro MD, Schluter D, Kingsley DM. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol. (2004) 2:635–641.[Web of Science]

    Cresko WA, Amores A, Wilson C, Murphy J, Currey M, Philips P, Bell MA, Kimmel CB, Postlethwait JH. Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proc Natl Acad Sci USA (2004) 101:6050–6055.[Abstract/Free Full Text]

    Eizirik E, Yuhki N, Johnson WE, Menotti-Raymon M, Hannah SS, O'Brien SJ. Molecular genetics and evolution of melanism in the cat family. Curr Biol. (2003) 13:448–453.[CrossRef][Web of Science][Medline]

    Foster SA, Baker JA. Evolution in parallel: new insights from a classic system. Trends Ecol Evol. (2004) 19:456–459.[CrossRef][Medline]

    Gibson G. The synthesis and evolution of a supermodel. Science (2005) 307:1890–1891.[Abstract/Free Full Text]

    Giles N. The possible role of environmental calcium levels during the evolution of phenotypic diversity in Outer Hebridean populations of three-spined stickleback, Gasterosteus aculeatus. J Zool (1983) 199:535–544.[Web of Science]

    Gompel N, Carroll SB. Genetic mechanisms and constraint governing the evolution of correlated traits in drosophilid flies. Nature (2003) 424:931–934.[CrossRef][Medline]

    Gompel N, Prud'homme B, Wittkopp PJ, Kassner VA, Carroll SB. Chance caught on the wing: cis-regulatory evolution and the origin of pigment patterns in Drosophila. Nature (2005) 433:481–487.[CrossRef][Medline]

    Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP. A single amino acid mutation contributes to adaptive beach mouse color pattern. Science (2006) 313:101–104.[Abstract/Free Full Text]

    Kingsley DM, Peichel CL. The molecular genetics of evolutionary change in sticklebacks. In: Biology of the three-spined stickleback—Ostlund-Nilsson S, Mayer I, Huntingford FA, eds. (2007) Boca Raton (FL): CRC Press. 41–81.

    Kingsley D, Zhu B, Osoegawa K, deJong PJ, Schein J, Marra M, Peichel C, Amemiya C, Schluter D, Balabhadra S, et al. New genomic tools for molecular studies of evolutionary change in sticklebacks. Behaviour (2004) 141:1331–1344.[CrossRef]

    Marcil A, Dumontier M, Chamberland M, Camper SA, Drouin J. Pitx1 and Pitx2 are required for development of hindlimb buds. Development (2003) 130:45–55.[Abstract/Free Full Text]

    Moodie GEE, Reimchen TE. Phenetic variation and habitat differences in Gasterosteus populations of the Queen Charlotte Islands. Syst Zool (1976) 25:49–61.[Medline]

    Mundy NI, Badcock NS, Hart T, Scribner K, Janssen K, Nadeau N. Conserved genetic basis of a quantitative plumage trait involved in mate choice. Science (2004) 303:1870–1873.[Abstract/Free Full Text]

    Nachman MW, Hoekstra HE, D'Agostino SL. The genetic basis of adaptive melanism in pocket mice. Proc Natl Acad Sci USA (2003) 100:5268–5273.[Abstract/Free Full Text]

    Orr HA. The genetic theory of adaptation: a brief history. Nat Rev Genet. (2005) 6:119–127.[CrossRef][Web of Science][Medline]

    Peichel CL. Fishing for the secrets of vertebrate evolution in threespine sticklebacks. Dev Dyn (2005) 234:815–823.[CrossRef][Web of Science][Medline]

    Peichel CL, Nereng KS, Ohgi KA, Cole BLE, Colosimo PF, Buerkle AC, Schluter D, Kingsley DM. The genetic architecture of divergence between threespine stickleback species. Nature (2001) 414:901–905.[CrossRef][Medline]

    Protas ME, Hersey C, Kochanek D, Zhou Y, Wilkens H, Jeffery WR, Zon LI, Borowsky R, Tabin CJ. Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nat Genet. (2006) 38:107–111.[CrossRef][Web of Science][Medline]

    Prud'homme B, Gompel N, Rokas A, Kassner VA, Williams TM, Yeh S-D, True JR, Carroll SB. Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene. Nature (2006) 440:1050–1053.[CrossRef][Medline]

    Reimchen TE. Spine deficiency and polymorphism in a population of Gasterosteus aculeatus: an adaptation to predators? Can J Zool (1980) 58:1232–1244.

    Römpler H, Rohland N, Lalueza-Fox C, Willerslev E, Kuznetsova T, Rabeder G, Bertranpetit J, Schöneberg T, Hofreiter M. Nuclear gene indicates coat-color polymorphism in mammals. Science (2006) 313:62.[Abstract/Free Full Text]

    Rosenblum EB, Hoekstra HE, Nachman MW. Adaptive reptile color variation and the evolution of the Mc1r gene. Evolution (2004) 58:1794–1808.[CrossRef][Web of Science][Medline]

    Shapiro MD, Bell MA, Kingsley DM. Parallel genetic origins of pelvic reduction in vertebrates. Proc Natl Acad Sci USA (2006) 103:13753–13758.[Abstract/Free Full Text]

    Shapiro MD, Marks ME, Peichel CL, Blackman BK, Nereng KS, Jónsson B, Schluter D, Kingsley DM. Genetic and developmental basis of evolutionary pelvic reduction in threespine stickleback. Nature (2004) 428:717–723.[CrossRef][Medline]

    Sucena E, Delon I, Payre F, Stern DL. Regulatory evolution of shavenbaby/ovo underlies multiple cases of morphological parallelism. Nature (2003) 424:935–938.[CrossRef][Medline]

    Theron E, Hawkins K, Bermingham E, Ricklefs RE, Mundy RI. The molecular basis of an avian plumage polymorphism in the wild: a melanocortin-1-receptor point mutation is perfectly associated with the melanic plumage morph of the bananaquit, Coereba flaveola. Curr Biol. (2001) 11:550–557.[CrossRef][Web of Science][Medline]

    Van Ooijen JW, Moer MP, Jansen RC, Maliepaard C. MapQTL 4.0: software for the calculation of QTL positions on genetic maps. (2002) Wageningen (The Netherlands): Plant Research International.

    Van Ooijen JW, Voorips RE. JoinMap 3.0: software for the calculation of genetic linkage maps. (2001) Wageningen (The Netherlands): Plant Research International.


Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
 ScienceHome page
Y. F. Chan, M. E. Marks, F. C. Jones, G. Villarreal Jr., M. D. Shapiro, S. D. Brady, A. M. Southwick, D. M. Absher, J. Grimwood, J. Schmutz, et al.
Adaptive Evolution of Pelvic Reduction in Sticklebacks by Recurrent Deletion of a Pitx1 Enhancer
Science, January 15, 2010; 327(5963): 302 - 305.
[Abstract] [Full Text] [PDF]

Home page
 Mol Biol EvolHome page
C. C. Steiner, H. Rompler, L. M. Boettger, T. Schoneberg, and H. E. Hoekstra
The Genetic Basis of Phenotypic Convergence in Beach Mice: Similar Pigment Patterns but Different Genes
Mol. Biol. Evol., January 1, 2009; 26(1): 35 - 45.
[Abstract] [Full Text] [PDF]

Home page
 Integr. Comp. Biol.Home page
C. J. Schneider
Exploiting genomic resources in studies of speciation and adaptive radiation of lizards in the genus Anolis
Integr. Comp. Biol., October 1, 2008; 48(4): 520 - 526.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
98/6/581    most recent
esm066v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrow Search for citing articles in:
ISI Web of Science (9)
Right arrowRequest Permissions
Google Scholar
Right arrow Articles by Coyle, S. M.
Right arrow Articles by Peichel, C. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Coyle, S. M.
Right arrow Articles by Peichel, C. L.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?