History

Research on D.americana: an historical perspective

A PubMed search on the 8th October 2010 with the words “Drosophila americana” revealed 110 articles, being 41 on Drosophila americana. Although, surely, not all relevant work on D. americana has been highlighted, the search results clearly indicate what have been the main research themes on D. americana.

When D. americana was first described, it was thought to be a subspecies of Drosophila virilis (see for instance, Hughes, 1939). Although the D. americana species status has been established prior to 1952, the subspecies status proposal is still surprising given the reported D. virilis/D. americanahybrid developmental problems (Heikkinen, 1992; Heikkinen et al., 1998; Nickel and Civetta, 2009; Sweigart, 2010a and b).

On the basis of the geographic pattern of a X/4 chromosomal fusion, D. americana was thought to be made of two subspecies (D. a. americana and D. a. texana), that would overlap in a large hybrid zone (see for instance, Hilton and Hey, 1996). Nevertheless, since 2006, there is no doubt that D. americana is a single species that shows a north-south gradient for several chromosomal rearrangements. Studies have been published regarding the evolutionary forces that maintain such chromosomal gradients (see for instance Vieira et al., 2006, Evans et al., 2007 or McAllister et al., 2008). Although debatable, since it seems to imply the existence of two subspecies, the D. a. americana and D. a. texana designations are still used in the literature to refer to individuals from the northernmost and southernmost range of the distribution (see for instance, Nickel and Civetta, 2009).

The view that D. americana was made of two subspecies that would overlap in a large hybrid zone meant that Drosophila a. americana has a neo-sex chromosome. Neo-sex chromosomes are rare in Drosophila and are considered to be an excellent model for the study of the evolution of the Y chromosome. In 1942, Stalker pointed out the lack of degeneration of the putative D. a. americana neo-sex chromosome, a finding that has been largely confirmed in subsequent molecular studies. Therefore, at large, there is no neo-sex chromosome in D. americana.

D. americana is native to United States where it has been independently evolving for approximately one My (Caletka and McAllister, 2004; Morales-Hojas et al., 2008). D. novamexicana is closely related to D. americana but it shows important phenotypic differences, and this has been explored in some studies (see for instance Wittkopp et al., 2003).

D. americana is widely distributed, from the Central and Eastern regions of the United States from the South (Texas to the states around the Gulf of Mexico) to the North of the country (from Montana to Maine) (Patterson and Stone, 1952). This species has been shown to have a high effective population size and low levels of population structure (Schäfer et al., 2006; Morales-Hojas et al., 2008). This feature has been explored when performing work on codon bias, for instance (Maside et al., 2004). The large phenotypic variation of this species regarding ecologically relevant traits is now being explored (see for instance, Wittkopp et al., 2010).

D. americana can now be widely used as a model species for comparative studies. Indeed, this species can be easily collected; for instance, in the last 10 years, the Bryant McAllister and the Jorge Vieira labs collected well over 500 D. americana individuals from most of the range of the distribution of this species; a large number of isofemale and isogenic D. americana strains are available at the McAllister and Vieira labs; this species shows a large effective population size and large phenotypic variation; the D. americana genome sequence has been determined, and the annotation will soon follow; markers for common chromosomal inversions and fusions are available; indel markers that can be cheaply typed in a large number of individuals are being developed by the Jorge Vieira lab (IBMC; Porto, Portugal); there is little or no population structure and polymorphism estimates based on a large number of loci are available; finally the phylogeny of the virilis group (where D. americana belongs) has been resolved with high confidence.

 

Title

Reference

Local adaptation for body color in Drosophila americana.

Wittkopp PJ, Smith-Winberry G, Arnold LL, Thompson EM, Cooley AM, Yuan DC, Song Q, McAllister BF. Heredity. 2010.

Simple Y-autosomal incompatibilities cause hybrid male sterility in reciprocal crosses between Drosophila virilis and D. americana.

Sweigart AL.Genetics. 2010. 184(3):779-87.

The genetics of postmating, prezygotic reproductive isolation between Drosophila virilis and D. americana.

Sweigart AL.Genetics. 2010. 184(2):401-10.

Reduced effectiveness of selection caused by a lack of recombination.

Betancourt AJ, Welch JJ, Charlesworth B. Curr Biol. 2009. 19(8):655-60.

An X chromosome effect responsible for asymmetric reproductive isolation between male Drosophila virilis and heterospecific females.

Nickel D, Civetta A.Genome. 2009. 52(1):49-56.

Patterns of natural selection at the Alcohol dehydrogenase gene of Drosophila americana.

Sheeley SL, McAllister BF. Fly (Austin). 2008. 2(5):243-6.

An old bilbo-like non-LTR retroelement insertion provides insight into the relationship of species of the virilis group.

Reis M, Vieira CP, Morales-Hojas R, Vieira J.Gene. 2008. 425(1-2):48-55.

[The relationships among the species of the Drosophila virilis group inferred from the gene Ras1 sequences]

Chekunova AI, Kulikov AM, Mikhaĭlovskiĭ SS, Lazebnyĭ OE, Lazebnaia IV, Mitrofanov VG. Genetika. 2008. 44(3):336-45.

Clinal distribution of a chromosomal rearrangement: a precursor to chromosomal speciation?

McAllister BF, Sheeley SL, Mena PA, Evans AL, Schlötterer C. Evolution. 2008. 62(8):1852-65.

Inferring the evolutionary history of Drosophila americana and Drosophila novamexicana using a multilocus approach and the influence of chromosomal rearrangements in single gene analyses.

Morales-Hojas R, Vieira CP, Vieira J. Mol Ecol. 2008. 17(12):2910-26.

 

Positive selection near an inversion breakpoint on the neo-X chromosome of Drosophila americana.

Evans AL, Mena PA, McAllister BF. Genetics. 2007. 177(3):1303-19.

Patterns of molecular variation and evolution in Drosophila americana and its relatives.

Maside X, Charlesworth B. Genetics. 2007. 176(4):2293-305.

Increased nucleotide diversity with transient Y linkage in Drosophila americana.

McAllister BF, Evans AL. PLoS One. 2006. 27;1:e112.

Patterns of microsatellite variation through a transition zone of a chromosomal cline in Drosophila americana.

Schäfer MA, Orsini L, McAllister BF, Schlötterer C. Heredity. 2006. 97(4):291-5.

On the location of the gene(s) harbouring the advantageous variant that maintains the X/4 fusion of Drosophila americana.

Vieira CP, Almeida A, Dias JD, Vieira J. Genet Res. 2006. 87(3):163-74.

Molecular characterization and evolution of the repeating units of histone genes in Drosophila americana: coexistence of quartet and quintet units in a genome.

Nagoda N, Fukuda A, Nakashima Y, Matsuo Y. Insect Mol Biol. 2005. 14(6):713-7.

A genealogical view of chromosomal evolution and species delimitation in the Drosophila virilis species subgroup.

Caletka BC, McAllister BF. Mol Phylogenet Evol. 2004. 33(3):664-70.

Dynamics and function of intron sequences of the wingless gene during the evolution of the Drosophila genus.

Costas J, Pereira PS, Vieira CP, Pinho S, Vieira J, Casares F. Evol Dev. 2004. 6(5):325-35.

A multilocus microsatellite phylogeny of the Drosophila virilis group.

Orsini L, Huttunen S, Schlötterer C. Heredity. 2004. 93(2):161-5.

Selection on codon usage in Drosophila americana.

Maside X, Lee AW, Charlesworth B. Curr Biol. 2004. 14(2):150-4.

Sequence differentiation associated with an inversion on the neo-X chromosome of Drosophila americana.

McAllister BF. Genetics. 2003. 165(3):1317-28.

Evolution of the GC content of the histone 3 gene in seven Drosophila species.

Matsuo Y. Genes Genet Syst. 2003. 78(4):309-18.

Inferences on the evolutionary history of the Drosophila americana polymorphic X/4 fusion from patterns of polymorphism at the X-linked paralytic and elav genes.

Vieira CP, Coelho PA, Vieira J. Genetics. 2003. 164(4):1459-69.

 

Drosophila pigmentation evolution: divergent genotypes underlying convergent phenotypes.

Wittkopp PJ, Williams BL, Selegue JE, Carroll SB. Proc Natl Acad Sci U S A. 2003. 100(4):1808-13.

In situ hybridisation analysis of the X-linked genes in the species of the virilis group of Drosophila.

Päällysaho S. Genetica. 2002.114(1):73-9.

Chromosomal and allelic variation in Drosophila americana: selective maintenance of a chromosomal cline.

McAllister BF. Genome. 2002. 45(1):13-21.

Evidence for selection at the fused1 locus of Drosophila americana.

Vieira J, McAllister BF, Charlesworth B. Genetics. 2001. 158(1):279-90.

Microsatellite analysis indicates genetic differentiation of the neo-sex chromosomes in Drosophila americana americana.

Schlötterer C. Heredity. 2000. 85(Pt 6):610-6.

Neutral evolution of the sex-determining gene transformer in Drosophila.

McAllister BF, McVean GA.Genetics. 2000. 154(4):1711-20.

Reduced sequence variability on the Neo-Y chromosome of Drosophila americana americana.

McAllister BF, Charlesworth B. Genetics. 1999. 153(1):221-33.

Adaptation to a starch environment and regulation of alpha-amylase in Drosophila.

Fujimoto J, Kanou C, Eguchi Y, Matsuo Y. Biochem Genet. 1999. 37(1-2):53-62.

The Y chromosomes of Drosophila lummei and D. novamexicana differ in fertility factors.

Heikkinen E, Lumme J.Heredity. 1998. 81 ( Pt 5):505-13.

Lack of degeneration of loci on the neo-Y chromosome of Drosophila americana americana.

Charlesworth B, Charlesworth D, Hnilicka J, Yu A, Guttman DS. Genetics. 1997. 145(4):989-1002.

DNA sequence variation at the period locus reveals the history of species and speciation events in the Drosophila virilis group.

Hilton H, Hey J. Genetics. 1996. 144(3):1015-25.

Sequence evolution of the Gpdh gene in the Drosophila virilis species group.

Tominaga H, Narise S. Genetica. 1995. 96(3):293-302.

Regulatory differences in developmental expression of alcohol dehydrogenase are related to interspecies differences in ethanol tolerance of Drosophila.

Ranganayakulu G, Reddy AR. Heredity. 1994. 72 ( Pt 4):374-83.

 

Genetic basis of reduced eyes in the hybrids of Drosophila virilis phylad species.

Heikkinen E. Hereditas. 1992. 117(3):275-85.

Chromosomal rearrangement In(2)TY and linkage maps of the second chromosome of Drosophila virilis.

Tsuno K, Yamaguchi O. Jpn J Genet. 1991. Feb;66(1):49-58.

Sites of the 5S ribosomal genes in Drosophila. I. The multiple clusters in the virilis group.

Wimber DE, Wimber DR. Genetics. 1977. 86(1):133-48.

Triploid Intersexuality in Drosophila Americana Spencer.

Stalker HD. Genetics. 1942. 27(5):504-18.

An Analysis of the Chromosomes of the Two Sub-Species Drosophila Virilis Virilis and Drosophila Virilis Americana.

Hughes RD. Genetics. 1939. 24(6):811-34.