FEMALE STERILITY IN HYBRIDS BETWEEN ANOPHELES GAMBIAE AND A. ARABIENSIS, AND THE CAUSES OF HALDANE'S RULE

Abstract Although F1 female hybrids between Anopheles gambiae and A. arabiensis are fully fertile, sterility is present in backcross females. Here we report the results of a study into the genetic basis of backcross female sterility. Using 23 markers, we performed quantitative trait loci (QTL) mapping analyses to identify chromosomal regions involved in hybrid female sterility. We found that female sterility in backcrosses in both directions is primarily caused by interspecific interactions between a heterozygous X chromosome and recessive autosomal factors. In addition, our data provide support for two theories implicated in Haldane's rule in a single taxon. A comparison with data from a previous study shows that male hybrid sterility QTL are present in higher numbers than female hybrid sterility QTL. Furthermore, autosomal female sterility factors tend to be recessive, supporting the dominance theory for female sterility. Finally, our data indicate a very large effect of the X chromosome from both species on hybrid female sterility, despite the fact that the X chromosome represents less than 9% of the genome. However, this could be the result of a lack of introgression of the X chromosome between A. gambiae and A. arabiensis, rather than a faster evolution of sterility factors on the X chromosome.

[1]  J. Powell,et al.  Differential introgression of chromsomal regions between Anopheles gambiae and An. arabiensis. , 2005, The American journal of tropical medicine and hygiene.

[2]  Matthew W. Hahn,et al.  Female-biased gene expression in the malaria mosquito Anopheles gambiae , 2005, Current Biology.

[3]  M. Noor,et al.  A TEST OF THE CHROMOSOMAL REARRANGEMENT MODEL OF SPECIATION IN DROSOPHILA PSEUDOOBSCURA , 2004, Evolution; international journal of organic evolution.

[4]  J. Powell,et al.  The Genetics of Inviability and Male Sterility in Hybrids Between Anopheles gambiae and An. arabiensis , 2004, Genetics.

[5]  M. Noor,et al.  USING COMPARATIVE GENOMIC DATA TO TEST FOR FAST-X EVOLUTION , 2004, Evolution; international journal of organic evolution.

[6]  D. Hartl,et al.  GENETIC DISSECTION OF HYBRID INCOMPATIBILITIES BETWEEN DROSOPHILA SIMULANS AND D. MAURITIANA.: III. HETEROGENEOUS ACCUMULATION OF HYBRID INCOMPATIBILITIES, DEGREE OF DOMINANCE, AND IMPLICATIONS FOR HALDANE—RULE , 2003, Evolution; international journal of organic evolution.

[7]  Rama S. Singh,et al.  Sex-linked mammalian sperm proteins evolve faster than autosomal ones. , 2003, Molecular biology and evolution.

[8]  J. Krzywinski,et al.  Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: Evidence from multilocus DNA sequence variation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[9]  D. Hartl,et al.  Genetic dissection of hybrid incompatibilities between Drosophila simulans and D. mauritiana. I. Differential accumulation of hybrid male sterility effects on the X and autosomes. , 2003, Genetics.

[10]  Colin D. Meiklejohn,et al.  Sex-Dependent Gene Expression and Evolution of the Drosophila Transcriptome , 2003, Science.

[11]  D. Presgraves,et al.  A fine-scale genetic analysis of hybrid incompatibilities in Drosophila. , 2003, Genetics.

[12]  N. Barton,et al.  ACCUMULATING POSTZYGOTIC ISOLATION GENES IN PARAPATRY: A NEW TWIST ON CHROMOSOMAL SPECIATION , 2003, Evolution; international journal of organic evolution.

[13]  Justen Andrews,et al.  Paucity of Genes on the Drosophila X Chromosome Showing Male-Biased Expression , 2003, Science.

[14]  W. Swanson,et al.  Reproductive Protein Evolution , 2002 .

[15]  Jian Wang,et al.  The Genome Sequence of the Malaria Mosquito Anopheles gambiae , 2002, Science.

[16]  W. Swanson,et al.  A test for faster X evolution in Drosophila. , 2002, Molecular biology and evolution.

[17]  M. Noor,et al.  Chromosomal inversions and the reproductive isolation of species , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. Noor,et al.  Consequences of recombination rate variation on quantitative trait locus mapping studies. Simulations based on the Drosophila melanogaster genome. , 2001, Genetics.

[19]  N. Besansky,et al.  Patterns of DNA sequence variation in chromosomally recognized taxa of Anopheles gambiae: evidence from rDNA and single‐copy loci , 2001, Insect molecular biology.

[20]  H. A. Orr,et al.  Dominance, epistasis and the genetics of postzygotic isolation. , 2000, Genetics.

[21]  C. Wu,et al.  Genetic analysis of speciation by means of introgression into Drosophila melanogaster. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Z. Zeng,et al.  Multiple interval mapping for quantitative trait loci. , 1999, Genetics.

[23]  Keith A. Gardner,et al.  Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species. , 1999, Genetics.

[24]  Y. Touré,et al.  The distribution and inversion polymorphism of chromosomally recognized taxa of the Anopheles gambiae complex in Mali, West Africa. , 1998, Parassitologia.

[25]  H. A. Orr,et al.  Haldane's rule in taxa lacking a hemizygous X. , 1998, Science.

[26]  J. Powell,et al.  Multiple origins of cytologically identical chromosome inversions in the Anopheles gambiae complex. , 1998, Genetics.

[27]  R. Hunt,et al.  The Anopheles gambiae complex: a new species from Ethiopia. , 1998, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[28]  H. A. Orr,et al.  HALDANE'S RULE , 1997 .

[29]  J. Powell,et al.  Selective introgression of paracentric inversions between two sibling species of the Anopheles gambiae complex. , 1997, Genetics.

[30]  C. Wu,et al.  The genetics of reproductive isolation in the Drosophila simulans clade: X vs. autosomal effects and male vs. female effects. , 1996, Genetics.

[31]  M. Benedict,et al.  An integrated genetic map of the African human malaria vector mosquito, Anopheles gambiae. , 1996, Genetics.

[32]  H. A. Orr,et al.  Dominance and Haldane's rule. , 1996, Genetics.

[33]  J. True,et al.  A genome-wide survey of hybrid incompatibility factors by the introgression of marked segments of Drosophila mauritiana chromosomes into Drosophila simulans. , 1996, Genetics.

[34]  A. Civetta,et al.  High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species , 1995, Journal of Molecular Evolution.

[35]  J. Werren,et al.  HYBRID BREAKDOWN BETWEEN TWO HAPLODIPLOID SPECIES: THE ROLE OF NUCLEAR AND CYTOPLASMIC GENES. , 1995 .

[36]  J. Werren,et al.  HYBRID BREAKDOWN BETWEEN TWO HAPLODIPLOID SPECIES: THE ROLE OF NUCLEAR AND CYTOPLASMIC GENES , 1995, Evolution; international journal of organic evolution.

[37]  H. A. Orr,et al.  The dominance theory of Haldane's rule. , 1995, Genetics.

[38]  F. Sperling SEX-LINKED GENES AND SPECIES DIFFERENCES IN LEPIDOPTERA , 1994, The Canadian Entomologist.

[39]  Chung-I Wu,et al.  Evidence for complex genic interactions between conspecific chromosomes underlying hybrid female sterility in the Drosophila simulans clade. , 1994, Genetics.

[40]  Z. Zeng Precision mapping of quantitative trait loci. , 1994, Genetics.

[41]  H. A. Orr,et al.  A MATHEMATICAL MODEL OF HALDANE'S RULE , 1993, Evolution; international journal of organic evolution.

[42]  Andrew W. Davis Evolution of Postmating Reproductive Isolation: The Composite Nature of Haldane's Rule and Its Genetic Bases , 1993, The American Naturalist.

[43]  J. Beier,et al.  Species composition of the Anopheles gambiae complex (diptera: Culicidae) at two sites in western Kenya. , 1991, Journal of medical entomology.

[44]  H. A. Orr,et al.  The genetics of postzygotic isolation in the Drosophila virilis group. , 1989, Genetics.

[45]  M. Daly,et al.  MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. , 1987, Genomics.

[46]  H. A. Orr,et al.  Genetics of male and female sterility in hybrids of Drosophila pseudoobscura and D. persimilis. , 1987, Genetics.

[47]  Nicholas H. Barton,et al.  The Relative Rates of Evolution of Sex Chromosomes and Autosomes , 1987, The American Naturalist.

[48]  W. Rice SEX CHROMOSOMES AND THE EVOLUTION OF SEXUAL DIMORPHISM , 1984, Evolution; international journal of organic evolution.

[49]  U. Schäfer Sterility in Drosophila hydei x D. neohydei hybrids , 1978, Genetica.

[50]  R. Hunt,et al.  The crossing and chromosome characteristics of a new, sixth species in the Anopheles gambiae complex. , 1973, Parassitologia.

[51]  D. Lindsley,et al.  The genetic control of spermatogenesis in Drosophila , 1972 .

[52]  G. Mason,et al.  The Anopheles gambiae complex , 1965 .

[53]  G. Davidson THE FIVE MATING-TYPES IN THE ANOPHELES GAMBIAE COMPLEX. , 1964, Rivista di malariologia.

[54]  G. Davidson Anopheles gambiae Complex , 1962, Nature.

[55]  T. Dobzhansky STUDIES ON HYBRID STERILITY. 11. LOCALIZATION OF STERILITY FACTORS I N DROSOPHILA PSEUDOOBSCURA HYBRIDS , 2003 .

[56]  F. Tripet,et al.  Frequency of multiple inseminations in field-collected Anopheles gambiae females revealed by DNA analysis of transferred sperm. , 2003, The American journal of tropical medicine and hygiene.

[57]  D. Hartl,et al.  GENETIC DISSECTION OF HYBRID INCOMPATIBILITIES BETWEEN DROSOPHILA SIMULANS AND D. MAURITIANA. III. HETEROGENEOUS ACCUMULATION OF HYBRID INCOMPATIBILITIES, DEGREE OF DOMINANCE, AND IMPLICATIONS FOR HALDANE'S RULE , 2003 .

[58]  R. Doerge,et al.  Permutation tests for multiple loci affecting a quantitative character. , 1996, Genetics.

[59]  R. P. Marchand Field Observations On Swarming and Mating in Anopheles Gambiae Mosquitoes in Tanzania1 , 1983 .

[60]  M. Coluzzi,et al.  Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. , 1979, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[61]  G. White Anopheles gambiae complex and disease transmission in Africa. , 1974, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[62]  G. White,et al.  The crossing characteristics of a new, sixth species in the Anopheles gambiae complex. , 1972, Transactions of the Royal Society of Tropical Medicine and Hygiene.