Abstract
The role of sexual selection in driving the rapid evolution of male reproductive proteins has been tested in a wide variety of organisms. Sperm competition is a form of postmating sexual selection that can contribute to reproductive isolation between species by biasing the proportion of progeny fathered by conspecific over heterospecific males. This phenomenon is known as conspecific sperm precedence (CSP). A previous quantitative trait loci study between Drosophila simulans and D. sechellia identified a locus associated with CSP within the second chromosome centered at the 53 cytogenetic map position. Male accessory gland proteins (ACPs) are associated with triggering postmating physiological responses in D. melanogaster females that can contribute to differential male reproductive success. Moreover, a large number of ACPs evolve rapidly and under positive selection among closely-related species of Drosophila. Here we have sequenced five candidate Acp genes (Acp53C14a, Acp53C14b, Acp53C14c, Acp53Ea and Acp54A1) within the previously mapped D. simulans–D. sechellia CSP locus from different D. simulans and D. sechellia strains. Polymorphism data analysis shows evidence of a selective sweep at Acp53Ea within D. simulans. In the context of CSP, the combined use of polymorphism and interspecies sequence divergence shows that Acp53C14c gene tree topology separates D. simulans and D. sechellia. Moreover, Acp53C14c is the only gene showing evidence of positive selection with five fixed amino acid substitutions between species. Our results highlight Acp53C14c as a candidate gene for future gene targeting studies to elucidate its role in CSP between D. simulans and D. sechellia.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10709-014-9800-7/MediaObjects/10709_2014_9800_Fig1_HTML.gif)
Similar content being viewed by others
References
Abascal F, Zardoya R, Posada D (2005) ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21:2104–2105
Avila FW, Wolfner MF (2009) Acp36DE is required for uterine conformational changes in mated Drosophila females. Proc Natl Acad Sci USA 106:15796–15800
Avila FW, Sirot LK, LaFlamme BA, Rubinstein CD, Wolfner MF (2011) Insect seminal fluid proteins: identification and function. Annu Rev Entomol 56:21–40
Bassett AR, Tibbit C, Ponting CP, Liu JL (2013) Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Rep 4:220–228
Bromberg Y, Rost B (2007) SNAP: predict effect of non-synonymous polymorphisms on function. Nucl Acids Res 35:3823–3835
Chapman T (2008) The soup in my fly: evolution, form and function of seminal fluid proteins. PLoS Biol 6:e179
Civetta A (2003) Shall we dance or shall we fight? Using DNA sequence data to untangle controversies surrounding sexual selection. Genome 46:925–929
Civetta A, Singh RS (1995) High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species. J Mol Evol 41:1085–1095
Civetta A, Waldrip-Dail HM, Clark AG (2002) An introgression approach to mapping differences in mating success and sperm competitive ability in Drosophila simulans and D. sechellia. Genet Res 79:65–74
Clark AG, Aguadé M, Prout T, Harshman LG, Langley CH (1995) Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics 139:189–201
Clark NL, Aagaard JE, Swanson WJ (2006) Evolution of reproductive proteins from animals and plants. Reproduction 131:11–22
Fay JC, Wu CI (2000) Hitchhiking under positive Darwinian selection. Genetics 155:1405–1413
Fiumera AC, Dumont BL, Clark AG (2005) Sperm competitive ability in Drosophila melanogaster associated with variation in male reproductive proteins. Genetics 169:243–257
Fiumera AC, Dumont BL, Clark AG (2007) Associations between sperm competition and natural variation in male reproductive genes on the third chromosome of Drosophila melanogaster. Genetics 176:1245–1260
Gratz SJ, Wildonger J, Harrison MM, O’Connor-Giles KM (2013) CRISPR/Cas9-mediated genome engineering and the promise of designer flies on demand. Fly (Austin) 7:249–255
Gratz SJ, Ukken FP, Rubinstein CD, Thiede G, Donohue LK, Cummings AM, O’Connor-Giles KM (2014) Highly specific and efficient CRISPR/Cas9-catalyzed homology-directed repair in Drosophila. Genetics 196:961–971
Haerty W, Jagadeeshan S, Kulathinal RJ, Wong A, Ravi Ram K, Sirot LK, Levesque L, Artieri CG, Wolfner MF, Civetta A, Singh RS (2007) Evolution in the fast lane: rapidly evolving sex-related genes in Drosophila. Genetics 177:1321–1335
Howard DJ, Gregory P, Chu J, Cain M (1998) Conspecific sperm precedence is an effective barrier to hybridization between closely related species. Evolution 52:511–516
Larson EL, Hume GL, Andrés JA, Harrison RG (2012) Post-mating prezygotic barriers to gene exchange between hybridizing field crickets. J Evol Biol 25:174–186
Levesque L, Brouwers B, Sundararajan V, Civetta A (2010) Third chromosome candidate genes for conspecific sperm precedence between D. simulans and D. mauritiana. BMC Genet 11:21
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459–473
Manier MK, Lüpold S, Belote JM, Starmer WT, Berben KS, Ala-Honkola O, Collins WF, Pitnick S (2013) Postcopulatory sexual selection generates speciation phenotypes in Drosophila. Curr Biol 23:1853–1862
Matsubayashi KW, Katakura H (2009) Contribution of multiple isolating barriers to reproductive isolation between a pair of phytophagous ladybird beetles. Evolution 63:2563–2580
McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654
Mueller JL, Linklater JR, Ravi Ram K, Chapman T, Wolfner MF (2008) Targeted gene deletion and phenotypic analysis of the Drosophila melanogaster seminal fluid protease inhibitor Acp62F. Genetics 178:1605–1614
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426
Price CS (1997) Conspecific sperm precedence in Drosophila. Nature 388:663–666
Price CS, Kim CH, Posluszny J, Coyne JA (2000) Mechanisms of conspecific sperm precedence in Drosophila. Evolution 54:2028–2037
Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
Rugman-Jones PF, Eady PE (2007) Conspecific sperm precedence in Callosobruchus subinnotatus (Coleoptera: Bruchidae): mechanisms and consequences. Proc Biol Sci 274:983–988
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729
Thomas S, Singh RS (1992) A comprehensive study of genic variation in natural populations of Drosophila melanogaster. VII. Varying rates of genic divergence as revealed by two-dimensional electrophoresis. Mol Biol Evol 9:507–525
Tyler F, Harrison XA, Bretman A, Veen T, Rodríguez-Muñoz R, Tregenza T (2013) Multiple post-mating barriers to hybridization in field crickets. Mol Ecol 22:1640–1649
Vicario S, Moriyama EN, Powell JR (2007) Codon usage in twelve species of Drosophila. BMC Evol Biol 7:226
Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276
Wong A, Rundle H (2013) Selection on the Drosophila seminal fluid protein Acp62F. Ecol Evol 3:1942–1950
Wong A, Wolfner MF (2012) Evolution of Drosophila seminal proteins and their networks. In: Singh RS, Xu J, Kulathinal RJ (eds) Rapidly evolving genes and genetic systems, 1st edn. Oxford University Press, Oxford, pp 144–152
Wong A, Albright SN, Giebel JD, Ram KR, Ji S, Fiumera AC, Wolfner MF (2008) A role for Acp29AB, a predicted seminal fluid lectin, in female sperm storage in Drosophila melanogaster. Genetics 180:921–931
Acknowledgments
This work was supported by an NSERC Individual Discovery Grant to A. Civetta. A. Reimer was partially supported by an NSERC Undergraduate Student Research Award (USRA).
Conflict of interest
None.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Civetta, A., Reimer, A. Positive selection at a seminal fluid gene within a QTL for conspecific sperm precedence. Genetica 142, 537–543 (2014). https://doi.org/10.1007/s10709-014-9800-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-014-9800-7