Genetic Divergence in Adaptive Characters Between Sympatric Species of Stickleback

Hatfield, Todd

doi:10.1086/286036

Cited by 108 publications

(110 citation statements)

References 64 publications

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“…Our results corroborate earlier work documenting inbreeding and genetic coadaptation in Drosophila (Wallace 1953;Brnic 1954;Wallace and Vetukhiv 1955;Anderson 1968) and conform to more recent studies using marker assisted techniques (Clegg et al 1978;Cavener and Clegg 1981;Burton 1987Burton , 1990Hard et al 1992Hard et al , 1993Palapoli and Wu 1994;Doebley et al 1995;Lark et al 1995;Rieseberg et al 1995;Armbruster et al 1997;Hatfield 1997;Li et al 1997;Routman and Cheverud 1997) and others (reviewed in Whitlock et al 1995;Fenster et al 1997). Our observation of epistasis contributing to divergence at a very local scale has also been observed in a number of other studies (Templeton et al 1976;Price and Waser 1979;Burton 1987Burton , 1990Waser andPrice 1989, 1994;Parker 1992;Deng and Lynch 1996).…”

Section: Contribution Of Epistasis To Population Genetic Differentiationsupporting

confidence: 92%

Population Differentiation in an Annual Legume: Genetic Architecture

Fenster¹,

Galloway²

2000

Evolution

217

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Abstract. The presence or absence of epistasis, or gene interaction, is explicitly assumed in many evolutionary models. Although many empirical studies have documented a role of epistasis in population divergence under laboratory conditions, there have been very few attempts at quantifying epistasis in the native environment where natural selection is expected to act. In addition, we have little understanding of the frequency with which epistasis contributes to the evolution of natural populations. In this study we used a quantitative genetic design to quantify the contribution of epistasis to population divergence for fitness components of a native annual legume, Chamaecrista fasciculata. The design incorporated the contrast of performance of F 2 and F 3 segregating progeny of 18 interpopulation crosses with the F 1 and their parents. Crosses were conducted between populations from 100 m to 2000 km apart. All generations were grown for two seasons in the natural environment of one of the parents. The F 1 often outperformed the parents. This F 1 heterosis reveals population structure and suggests that drift is a major contributor to population differentiation. The F 2 generation demonstrated that combining genes from different populations can sometimes have unexpected positive effects. However, the F 3 performance indicated that combining genes from different populations decreased vigor beyond that due to the expected loss of heterozygosity. Combined with previous data, our results suggest that both selection and drift contribute to population differentiation that is based on epistatic genetic divergence. Because only the F 3 consistently expressed hybrid breakdown, we conclude that the epistasis documented in our study reflects interactions among linked loci.

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Section: Contribution Of Epistasis To Population Genetic Differentiationsupporting

confidence: 92%

Population Differentiation in an Annual Legume: Genetic Architecture

Fenster¹,

Galloway²

2000

Evolution

217

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“…To examine the influence of different genetic regions on trophic morphology, we counted the number of both long and short gill rakers on the first gill arch of all progeny from the Priest Lake cross (Figure 3b). No major QTL were found influencing the number of long gill rakers in the cross, consistent with previous biometrical studies suggesting that gill raker number may be based on a large number of genes of small effect 14,15 . In contrast, the number of short gill rakers is influenced by two QTL that map to separate linkage groups.…”

supporting

confidence: 90%

The genetic architecture of divergence between threespine stickleback species

Peichel

Nereng

Ohgi

et al. 2001

Nature

446

514

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The genetic and molecular basis of morphological evolution is poorly understood, particularly in vertebrates. Genetic studies of the differences between naturally occurring vertebrate species have been limited by the expense and difficulty of raising large numbers of animals and the absence of molecular linkage maps for all but a handful of laboratory and domesticated animals. We have developed a genome-wide linkage map for the threespine stickleback (Gasterosteus aculeatus), an extensively studied teleost fish that has undergone rapid divergence and speciation since the melting of glaciers 15,000 years ago 1 The benthic species feeds on invertebrates near shore and has a great reduction in the amount of body armor, increased body depth, and a decreased number of gill rakers for filtering ingested food. The limnetic species more closely resembles an ancestral marine fish, with more extensive body armor, a longer and more streamlined body, and an increased number of gill rakers. Despite reproductive isolation between the two species in the wild 3-6 , it is possible to establish productive matings between the two species under laboratory conditions 2 . The resulting F1 hybrids are viable and fertile, making it possible to carry out a formal genetic analysis of the number and location of loci responsible for the adaptive morphological differences between these naturally occurring vertebrate species.To develop resources for genome-wide linkage mapping in Gasterosteus aculeatus, we used large-scale library screening and sequencing to identify a collection of genomic and cDNA clones containing microsatellite repeat sequences. Initially, we sequenced of 192 kb of random genomic clones and showed that CA dinucleotides were the most common form of microsatellite in sticklebacks, occurring approximately once every 14 kb. We subsequently screened genomic and cDNA libraries with a (GT) 15 probe, sequenced 3560 clones, and identified 1176 new microsatellite loci. Primers flanking 410 new and 18 previously identified microsatellites 7-9 were designed and used to type a genetic cross between the benthic and limnetic species from Priest Lake, British Columbia (Figure 1). For this cross, an individual Priest benthic female was mated with a single Priest limnetic male, and a single F1 male (B 1 L 1 ) was crossed to a second Priest benthic female (B 2 B 3 ) to generate 103 progeny. Of the 281 markers that amplified robust bands from the F1 and benthic parent, 227 (81%) were polymorphic, and therefore informative, in one or both parents. Higher rates of polymorphism were seen in the F1 male than the benthic female parent (71% vs. 57% of 281 markers), consistent with a greater level of genetic diversity between the distinct populations of benthic and limnetic fish than within the benthic population.The segregation patterns of the 227 informative markers were scored on 92 progeny from the cross, and the 20,884 resulting genotypes were analyzed for linkage using JoinMap software 10 . The markers were ordered into 26 linkage groups co...

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“…Our study also contributes to the growing body of literature that describes the importance of non-additive gene action for evolutionary processes such as adaptation and speciation [19,43,46]. Our results suggest that higher-order gene interactions may also be important in determining the outcome of hybridization between species in secondary contact, because some of the most important determinants of salamander fitness ( i.e ., survival and Tmet) demonstrated significant non-additive inheritance.…”

Section: Discussionmentioning

confidence: 51%

“…Many previous studies have documented phenotypic differences arising from multiple genes acting additively on phenotypic traits [43-45], and our analyses add another example to this body of work. Our study also contributes to the growing body of literature that describes the importance of non-additive gene action for evolutionary processes such as adaptation and speciation [19,43,46].…”

Section: Discussionmentioning

confidence: 69%

Retention of low-fitness genotypes over six decades of admixture between native and introduced tiger salamanders

Johnson

Fitzpatrick

Shaffer

2010

BMC Evolutionary Biology

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BackgroundIntroductions of non-native tiger salamanders into the range of California tiger salamanders have provided a rare opportunity to study the early stages of secondary contact and hybridization. We produced first- and second-generation hybrid salamanders in the lab and measured viability among these early-generation hybrid crosses to determine the strength of the initial barrier to gene exchange. We also created contemporary-generation hybrids in the lab and evaluated the extent to which selection has affected fitness over approximately 20 generations of admixture. Additionally, we examined the inheritance of quantitative phenotypic variation to better understand how evolution has progressed since secondary contact.ResultsWe found significant variation in the fitness of hybrids, with non-native backcrosses experiencing the highest survival and F2 hybrids the lowest. Contemporary-generation hybrids had similar survival to that of F2 families, contrary to our expectation that 20 generations of selection in the wild would eliminate unfit genotypes and increase survival. Hybrid survival clearly exhibited effects of epistasis, whereas size and growth showed mostly additive genetic variance, and time to metamorphosis showed substantial dominance.ConclusionsBased on first- and second- generation cross types, our results suggest that the initial barrier to gene flow between these two species was relatively weak, and subsequent evolution has been generally slow. The persistence of low-viability recombinant hybrid genotypes in some contemporary populations illustrates that while hybridization can provide a potent source of genetic variation upon which natural selection can act, the sorting of fit from unfit gene combinations might be inefficient in highly admixed populations. Spatio-temporal fluctuation in selection or complex genetics has perhaps stalled adaptive evolution in this system despite selection for admixed genotypes within generations.

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Genetic Divergence in Adaptive Characters Between Sympatric Species of Stickleback

Cited by 108 publications

References 64 publications

Population Differentiation in an Annual Legume: Genetic Architecture

Population Differentiation in an Annual Legume: Genetic Architecture

The genetic architecture of divergence between threespine stickleback species

Retention of low-fitness genotypes over six decades of admixture between native and introduced tiger salamanders

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