Alternative reproductive tactics and sex-biased gene expression: the study of the bulb mite transcriptome

Abstract

The sexes experience different selective pressures, which can lead to highly divergent phenotypes that are achieved via sex-biased gene expression. The effect of sexual dimorphism on the degree of sex-bias in gene expression can be studied in species characterized by sexually selected alternative male phenotypes. We analyzed gene expression in the bulb mite Rhizoglyphus robini (Acari, Acaridae), in which more sexually dimorphic, aggressive fighter males, possessing thickened legs of the third pair which are used to kill rivals, coexist with unarmored scrambler males. We sequenced transcriptomes of adult females and both types of males and de-novo assembled 114,456 transcriptome-based gene models (TGMs). Significantly more TGMs had male-biased expression than female-biased expression. Among TGMs that were over expressed in one, but not both, male morphs (compared to expression in females), we found about four times more fighter-biased genes than scrambler-biased genes. This demonstrates that the degree of expression bias reflects the degree of sexually selected dimorphism. However, the number of sex-biased genes was much higher than the number of genes differentially expressed between male morphs, and most male-biased genes were shared between morphs, suggesting that selection pressures act similarly on males irrespective of their morph. Furthermore, we found that male-biased genes evolved at a faster rate than female-biased genes, as evidenced by a higher rate of both gene-turnover and amino acid substitution, indicating that sexual selection, acting more strongly on males, accelerates the rate of molecular evolution. Interestingly, gene turnover was relatively higher, but amino acid substitution rate relatively lower among fighter-biased genes, suggesting that different components of sexual selection may have different effects on the evolution of sex-biased genes.

References Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403–410. Andersson, M. B. 1994. Sexual selection. Princeton Univ. Press, Princeton, NJ. Arnqvist, G. and L. Rowe. 2005. Sexual conflict. Princeton Univ. Press, Princeton, NJ. Assis, R., Q. Zhou, and D. Bachtrog. 2012. Sex-biased transcriptome evolution in drosophila. Genome Biol. Evol. 4:1189–1200. Bairoch, A., U. Consortium, L. Bougueleret, S. Altairac, V. Amendolia, A. Auchincloss, et al. 2009. The universal protein resource (UniProt) 2009. Nucleic Acids Res. 37:D169–D174. Begun, D. J., P. Whitley, B. L. Todd, H. M. Waldrip-Dail, and A. G. Clark. 2000. Molecular population genetics of male accessory gland proteins in drosophila. Genetics 156:1879–1888. Birney, E., M. Clamp, and R. Durbin. 2004. GeneWise and genomewise. Genome Res. 14:988–995. Brockmann, H. J. 2001. The evolution of alternative strategies and tactics. Adv. Study Behav. 30:1–51. Chapman, T., L. F. Liddle, J. M. Kalb, M. F. Wolfner, and L. Partridge. 1995. Cost of mating in Drosophila melanogaster females is mediated by male accessory-gland products. Nature 373:241–244. Chapman, T., G. Arnqvist, J. Bangham, and L. Rowe. 2003. Sexual conflict. Trends Ecol. Evol. 18:41–47. Chen, P. S., E. Stummzollinger, T. Aigaki, J. Balmer, M. Bienz, and P. Bohlen. 1988. A male accessory-gland peptide that regulates reproductive-behavior of female Drosophila-melanogaster. Cell 54:291–298. Clark, A. G., M. Aguade, T. Prout, L. G. Harshman, and C. H. Langley. 1995. Variation in sperm sisplacement and its sssociation with accessory-gland protein loci in Drosophila melanogaster. Genetics 139:189–201. Conesa, A., S. Gotz, J. M. Garcia-Gomez, J. Terol, M. Talon, and M. Robles. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. Cox, M. P., D. A. Peterson, and P. J. Biggs. 2010. SolexaQA: At-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinformatics 11:485. Dabert, M., W. Witalinski, A. Kazmierski, Z. Olszanowski, and J. Dabert. 2010. Molecular phylogeny of acariform mites (Acari, Arachnida): strong conflict between phylogenetic signal and long-branch attraction artifacts. Mol. Phylogenet. Evol. 56:222–241. Duret, L. and D. Mouchiroud. 2000. Determinants of substitution rates in mammalian genes: expression pattern affects selection intensity but not mutation rate. Mol. Biol. Evol. 17:68–74. Ekblom, R., C. N. Balakrishnan, T. Burke, and J. Slate. 2010. Digital gene expression analysis of the zebra finch genome. BMC Genomics 11. Ellegren, H. and J. Parsch. 2007. The evolution of sex-biased genes and sex-biased gene expression. Nat. Rev. Genet. 8:689–698. Gentleman, R. C., V. J. Carey, D. M. Bates, B. Bolstad, M. Dettling, S. Dudoit, et al. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80. Grabherr, M. G., B. J. Haas, M. Yassour, J. Z. Levin, D. A. Thompson, I. Amit, et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29:644–652. Gross, M. R. 1996. Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol. Evol. 11:A92–A98. Haerty, W., S. Jagadeeshan, R. J. Kulathinal, A. Wong, K. R. Ram, L. K. Sirot, et al. 2007. Evolution in the fast lane: rapidly evolving sex-related genes in drosophila. Genetics 177:1321–1335. Heifetz, Y., O. Lung, E. A. Frongillo, and M. F. Wolfner. 2000. The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Curr. Biol. 10:99–102. Huang, X. Q. and A. Madan. 1999. CAP3: a DNA sequence assembly program. Genome Res. 9:868–877. Katoh, K., K. Misawa, K. Kuma, and T. Miyata. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30:3059–3066. Kersey, P. J., D. M. Staines, D. Lawson, E. Kulesha, P. Derwent, J. C. Humphrey, et al. 2012. Ensembl Genomes: an integrative resource for genome-scale data from non-vertebrate species. Nucleic Acids Res. 40:D91–D97. Langmead, B., C. Trapnell, M. Pop, and S. L. Salzberg. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. Li, B. and C. N. Dewey. 2011. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323. Li, W. Z. and A. Godzik. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659. Malone, J. H., D. L. Hawkins, and P. Michalak. 2006. Sex-biased gene expression in a ZW sex determination system. J. Mol. Evol. 63:427–436. Mank, J. E., L. Hultin-Rosenberg, E. Axelsson, and H. Ellegren. 2007. Rapid evolution of female-biased, but not male-biased, genes expressed in the avian brain. Mol. Biol. Evol. 24:2698–2706. Meisel, R. P. 2011. Towards a more nuanced understanding of the relationship between sex-biased gene expression and rates of protein-coding sequence evolution. Mol. Biol. Evol. 28:1893–1900. Mercer, T. R., M. E. Dinger, and J. S. Mattick. 2009. Long non-coding RNAs: insights into functions. Nat. Rev. Genet. 10:155–159. Oliveira, R. F., M. Taborsky, and H. Brockmann. 2008. Alternative reproductive tactics. Cambridge Univ. Press, Cambridge, U.K. Parisi, M., R. Nuttall, P. Edwards, J. Minor, D. Naiman, J. N. Lu, et al. 2004. A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults. Genome Biol. 5:R40. Parker, G. A. 1970. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45:525–567. Parker, G. A. 1979. Sexual selection and sexual conflict. Pp. 123–166 in M. S. Blum and N. A. Blum, eds. Sexual selection and reproductive competition in insects. Academic Press, New York, NY. Parsch, J. and H. Ellegren. 2013. The evolutionary causes and consequences of sex-biased gene expression. Nat. Rev. Genet. 14:83–87. Pennell, T. M. and E. H. Morrow. 2013. Two sexes, one genome: the evolutionary dynamics of intralocus sexual conflict. Ecol. Evol. 3:1819–1834. Pointer, M. A., P. W. Harrison, A. E. Wright, and J. E. Mank. 2013. Masculinization of gene expression is associated with exaggeration of male sexual dimorphism. PLoS Genet. 9:e1003697. Radwan, J. 1995. Male morph determination in two species of acarid mites. Heredity 74:669–673. Radwan, J. 2004. Effectiveness of sexual selection in removing mutations induced with ionizing radiation. Ecol. Lett. 7:1149–1154. Radwan, J. 2007. Sexual selection and conflict in the bulb mite, Rhizoglyphus robini (Astigmata: Acaridae). Exp. Appl. Acarol. 42:151–158. Radwan, J. 2009. Alternative mating tactics in acarid mites. Advances in the Study of Behavior 39:185–208. Radwan, J. and M. Siva-Jothy. 1996. The function of post-insemination mate association in the bulb mite, Rhizoglyphus robini. Anim. Behav. 52:651–657. Radwan, J., M. Czyz, M. Konior, and M. Kolodziejczyk. 2000. Aggressiveness in two male morphs of the bulb mite Rhizoglyphus robini. Ethology 106:53–62. Ranz, J. M., C. I. Castillo-Davis, C. D. Meiklejohn, and D. L. Hartl. 2003. Sex-dependent gene expression and evolution of the Drosophila transcriptome. Science 300:1742–1745. Robinson, M. D., D. J. McCarthy, and G. K. Smyth. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140. Small, C. M., G. E. Carney, Q. X. Mo, M. Vannucci, and A. G. Jones. 2009. A microarray analysis of sex- and gonad-biased gene expression in the zebrafish: evidence for masculinization of the transcriptome. BMC Genomics 10:579. Snell-Rood, E. C., J. D. Van Dyken, T. Cruickshank, M. J. Wade, and A. P. Moczek. 2010. Toward a population genetic framework of developmental evolution: the costs, limits, and consequences of phenotypic plasticity. BioEssays 32:71–81. Snell-Rood, E. C., A. Cash, M. V. Han, T. Kijimoto, J. Andrews, and A. P. Moczek. 2011. Developmental decoupling of alternative phenotypes: insights from the transcriptomes of horn-polyphenic beetles. Evolution 65:231–245. Swanson, W. J., and V. D. Vacquier. 2002. The rapid evolution of reproductive proteins. Nat. Rev. Genet. 3:137–144. Swanson, W. J., Z. H. Zhang, M. F. Wolfner, and C. F. Aquadro. 2001. Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc. Natl Acad. Sci. USA 98:2509–2514. Tilszer, M., K. Antoszczyk, N. Salek, E. Zajac, and J. Radwan. 2006. Evolution under relaxed sexual conflict in the bulb mite Rhizoglyphus robini. Evolution 60:1868–1873. Ulitsky, I. and D. P. Bartel. 2013. LincRNAs: genomics, evolution, and mechanisms. Cell 154:26–46. Van Dyken, J. D. and M. J. Wade. 2010. The genetic signature of conditional expression. Genetics 184:557–570. Vijay, N., J. W. Poelstra, A. Kunstner, and J. B. W. Wolf. 2013. Challenges and strategies in transcriptome assembly and differential gene expression quantification. A comprehensive in silico assessment of RNA-seq experiments. Mol. Ecol. 22:620–634. West-Eberhard, M. J. 1989. Phenotypic plasticity and the origins of diversity. Annu. Rev. Ecol. Syst. 20:249–278. Yang, Z. H. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24:1586–1591. Zhang, L. Q. and W. H. Li. 2004. Mammalian housekeeping genes evolve more slowly than tissue-specific genes. Mol. Biol. Evol. 21:236–239. Zhang, Z., T. M. Hambuch, and J. Parsch. 2004. Molecular evolution of sex-biased genes in Drosophila. Mol. Biol. Evol. 21:2130–2139. Zhang, Y., D. Sturgill, M. Parisi, S. Kumar, and B. Oliver. 2007. Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450:233–237.