The mate recognition protein gene mediates reproductive isolation and speciation in the Brachionus plicatilis cryptic species complex

BMC Evolutionary Biology

David B Mark Welch¹  Kristin E Gribble¹ 

[1] Marine Biological Laboratory, 7 MBL Street, Woods Hole, MA, 02543, USA

关键词: Gene family;    Concerted evolution;    Speciation;    Reproductive isolation;    Mate recognition;   

Others  :  1140663
DOI  :  10.1186/1471-2148-12-134

 received in 2012-04-23, accepted in 2012-07-23,  发布年份 2012

【 摘 要 】

Background

Chemically mediated prezygotic barriers to reproduction likely play an important role in speciation. In facultatively sexual monogonont rotifers from the Brachionus plicatilis cryptic species complex, mate recognition of females by males is mediated by the Mate Recognition Protein (MRP), a globular glycoprotein on the surface of females, encoded by the mmr-b gene family. In this study, we sequenced mmr-b copies from 27 isolates representing 11 phylotypes of the B. plicatilis species complex, examined the mode of evolution and selection of mmr-b, and determined the relationship between mmr-b genetic distance and mate recognition among isolates.

Results

Isolates of the B. plicatilis species complex have 1–4 copies of mmr-b, each composed of 2–9 nearly identical tandem repeats. The repeats within a gene copy are generally more similar than are gene copies among phylotypes, suggesting concerted evolution. Compared to housekeeping genes from the same isolates, mmr-b has accumulated only half as many synonymous differences but twice as many non-synonymous differences. Most of the amino acid differences between repeats appear to occur on the outer face of the protein, and these often result in changes in predicted patterns of phosphorylation. However, we found no evidence of positive selection driving these differences. Isolates with the most divergent copies were unable to mate with other isolates and rarely self-crossed. Overall the degree of mate recognition was significantly correlated with the genetic distance of mmr-b.

Conclusions

Discrimination of compatible mates in the B. plicatilis species complex is determined by proteins encoded by closely related copies of a single gene, mmr-b. While concerted evolution of the tandem repeats in mmr-b may function to maintain identity, it can also lead to the rapid spread of a mutation through all copies in the genome and thus to reproductive isolation. The mmr-b gene is evolving rapidly, and novel alleles may be maintained and increase in frequency via asexual reproduction. Our analyses indicate that mate recognition, controlled by MMR-B, may drive reproductive isolation and allow saltational sympatric speciation within the B. plicatilis cryptic species complex, and that this process may be largely neutral.

【 授权许可】

   
2012 Gribble and Mark Welch; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Coyne JA, Orr HA: Patterns of speciation in Drosophila. Evolution 1989, 43:362-381.
• [2]Coyne JA, Orr HA: "Patterns of speciation in Drosophila" revisited. Evolution 1997, 51:295-303.
• [3]Turner GF, Burrows MT: A model of sympatric speciation by sexual selection. Proceedings of the Royal Society of London B Biological Sciences 1995, 260:287-292.
• [4]Gavrilets S, Boake CR: On the evolution of premating isolation after a founder event. The American Naturalist 1998, 152:706-716.
• [5]Price TD, Bouvier MM: The evolution of F1 postzygotic incompatabilities in birds. Evolution 2002, 56:2083-2089.
• [6]Panhuis TM, Butlin R, Zuk M, Tregenza T: Sexual selection and speciation. Trends in Ecology and Evolution 2001, 16:364-371.
• [7]Roelofs WL: Chemistry of sex attraction. Proceedings of the National Academy of Sciences, USA 1995, 92:44-49.
• [8]Roelofs WL, Liu W, Hao G, Jiao H, Rooney AP, Linn CE Jr: Evolution of moth sex pheromones via ancestral genes. Proceedings of the National Academy of Sciences, USA 2002, 99:13621-13626.
• [9]Ferris P, Pavlovic C, Fabry S, Goodenough UW: Rapid evolution of sex-related genes in Chlamydomonas. Proceedings of the National Academy of Sciences, USA 1997, 94:8634-8639.
• [10]Hsueh YP, Shen W-C: A homolog of Ste6, the a-factor transporter in Saccharomyces cerevisiae, is required for mating but not for monkaryotic fruiting in Cryptococcus neoformans. Eukaryotic Cell 2005, 4:147-155.
• [11]Gilbert JJ, Thompson GA Jr: Alpha tocopherol control of sexuality and polymorphism in the rotifer Asplanchna. Science 1968, 159:734-736.
• [12]Lubzens E, Fishler R, Berdugo-White V: Induction of sexual reproduction and resting egg production in Brachionus plicatilisreared in sea water. Hydrobiologia 1980, 73:55-58.
• [13]Gilbert JJ: Specificity of crowding response that induces sexuality in the rotifer Brachionus. Limnology and Oceanography 2003, 48:1297-1303.
• [14]Stelzer C-P, Snell TW: Induction of sexual reproduction in Brachionus plicatilis (Monogononta, Rotifera) by a density dependent chemical cue. Limnology and Oceanography 2003, 48:939-943.
• [15]Fontaneto D, Kaya M, Herniou E, Barraclough TG: Extreme levels of hidden diversity in microscopic animals (Rotifera) revealed by DNA taxonomy. Molecular Phylogenetics and Evolution 2009, 53:182-189.
• [16]Gómez A, Serra M, Carvalho GR, Lunt DH: Speciation in ancient cryptic species complexes: Evidence from the molecular phylogeny of Brachionus plicatilis (Rotifera). Evolution 2002, 56:1431-1444.
• [17]Suatoni E, Vicario S, Rice S, Snell T, Acaccone A: An analysis of species boundaries and biogeographic patterns in a cryptic species complex: The rotifer–Brachionus plicatilis. Molecular Phylogenetics and Evolution 2006, 41:86-98.
• [18]Baer A, Langdon C, Mills S, Schulz C, Hamre K: Particle size preference, gut filling and evacuation rates of the rotifer Brachionus "Cayman" using polystyrene latex beads. Aquaculture 2008, 282:75-82.
• [19]Ciros-Pérez J, Gómez A, Serra M: On the taxonomy of three sympatric sibling species of the Brachionus plicatilis(Rotifera) complex from Spain, with the description ofB. ibericusn. sp. Journal of Plankton Research 2001, 23:1311-1328.
• [20]Fontaneto D, Giordani I, Melone G, Serra M: Disentangling the morphological stasis in two rotifer species of the Brachionus plicatilis species complex. Hydrobiologia 2007, 583:297-307.
• [21]Segers H: Annotated checklist of the rotifers (Phylum Rotifera), with notes on nomenclature, taxonomy and distribution. Zootaxa 2007, 1564:1-104.
• [22]Berrieman HK, Hunt DH, Gómez A: Behavioural reproductive isolation in a rotifer hybrid zone. Hydrobiologia 2005, 546:125-134.
• [23]Gilbert JJ: Contact chemoreception, mating behaviour, and sexual isolation in the rotifer genus Brachionus. Journal of Experimental Biology 1963, 40:625-641.
• [24]Snell TW, Rico-Martinez R, Kelly LN, Battle TE: Identification of a sex pheromone from a rotifer. Marine Biology 1995, 123:347-353.
• [25]Snell TW, Shearer TL, Smith HA, Kubanek J, Gribble KE, Mark Welch DB: Genetic determinants of mate recognition in Brachionus manjavacas (Rotifera). BMC Biology 2009, 7:60. BioMed Central Full Text
• [26]Snell TW, Stelzer C-P: Removal of surface glycoproteins and transfer among Brachionus species. Hydrobiologia 2005, 546:267-274.
• [27]Gribble KE, Snell TW, Mark Welch DB: Gene and protein structure of the mate recognition protein gene family in Brachionus manjavacas (Rotifera). Hydrobiologia 2011, 662:35-42.
• [28]Snell TW, Shearer TL, Smith HA: Exposure to dsRNA produces RNA interference in Brachionus manjavacas (Rotifera). Marine Biotechnology 2011, 13:264-274.
• [29]Zhang J, Nielsen R, Yang Z: Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Molecular Biology and Evolution 2005, 22:2472-2479.
• [30]Bielawski JP, Yang Z: A maximum likelihood method for detecting functional divergence at individual codon sites, with application to gene family evolution. Journal of Molecular Evolution 2004, 59:121-132.
• [31]Vacquier VD: Evolution of gamete recognition proteins. Science 1995, 281:1995-1998.
• [32]Nydam ML, Harrison RG: Reproductive protein evolution in two cryptic species of marine chordate. BMC Evolutionary Biology 2011, 11:18. BioMed Central Full Text
• [33]Martin SH, Wingfield BD, Wingfield MJ, Steenkamp ET: Causes and consequences of variability in peptide mating pheromones of ascomycete fungi. Molecular Biology and Evolution 2011.
• [34]Mayfield JA, Fiebig A, Johnstone SE, Preuss D: Gene families from the Arabadopsis thaliana pollen coat proteome. Science 2001, 292:2482-2485.
• [35]Swanson WJ, Vacquier VD: The rapid evolution of reproductive proteins. Nature Reviews Genetics 2002, 3:137-144.
• [36]Swanson WJ, Vacquier VD: Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein. Science 2011, 281:710-712.
• [37]McAllister BF, Werren JH: Evolution of tandemly repeated sequences: What happens and the end of an array? Journal of Molecular Evolution 1999, 48:469-481.
• [38]Nei M, Rooney AP: Concerted and birth-and-death evolution of multigene families. Annual Review of Genetics 2005, 39:121-152.
• [39]Ortells R, Gómez A, Serra M: Coexistence of cryptic rotifer species: ecological and genetic characterisation of Brachionus plicatilis. Freshwater Biology 2003, 48:2194-2202.
• [40]Ortells R, Snell TW, Gómez A, Serra M: Patterns of genetic differentiation in resting egg banks of a rotifer species complex in Spain. Archiv für Hydrobiologie 2000, 149:529-551.
• [41]Turelli M, Barton NH, Coyne JA: Theory and speciation. Trends in Ecology and Evolution 2001, 16:330-343.
• [42]Via S: Sympatric speciation in animals: the ugly duckling grows up. Trends in Ecology and Evolution 2001, 16:381-390.
• [43]Snell TW, Kubanek J, Carter W, Payne AB, Kim J, Hicks M, Stelzer C-P: A protein signal triggers sexual reproduction in Brachionus plicatilis (Rotifera). Marine Biology 2006, 149:763-773.
• [44]Gómez A, Carvalho GR, Lunt DH: Phylogeography and regional endemism of a passively dispersing zooplankter: mitochondrial DNA variation in rotifer resting egg banks. Proceedings of the Royal Society of London B Biological Sciences 2000, 267:2189-2197.
• [45]Mills S, Lunt DH, Gómez A: Global isolation by distance despite strong relational phylogeography in a small metazoan. BMC Evolutionary Biology 2007., 7 BioMed Central Full Text
• [46]Guillard RRL: Culture of phytoplankton for feeding marine invertebrates. In Culture of Marine Invertebrates. Edited by Smith WL, Chanley MH. New York, New York: Plenum Publishing Corporation; 1975.
• [47]Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R: DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 1994, 3:294-299.
• [48]Mark Welch DB: Evidence from a protein-coding gene that Acanthocephalans are Rotifers. Invertebrate Biology 2000, 19:17-26.
• [49]Huelsenbeck JP, Ronquist F: MRBAYES: Baesian inference of phylogeny. Bioinformatics 2001, 17:754-755.
• [50]Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
• [51]Gelman A, Rubin DB: Inference from iterative simulation using multiple sequences. Statistical Science 1992, 7:457-511.
• [52]Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R: DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003, 19:2496-2497.
• [53]Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 2011, 28:2731-2739.
• [54]Yang Z: PAML 4: a program package for phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 2007, 24:1586-1591.
• [55]Muse SV, Gaut BS: A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Molecular Biology and Evolution 1994, 11:715-724.
• [56]Garnier J, Osguthorpe D, Robson B: Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. Journal of Molecular Biology 1978, 120:97-120.
• [57]Cheng H, Sen TZ, Kloczkowski A, Margaritits D, Jernigan RL: Prediction of protein secondary structure by mining structural fragment database. Polymer 2005, 46:4314-4321.
• [58]Sen TZ, Cheng H, Kloczkowski A, Jernigan RL: A Consensus Data Mining secondary structure prediction by combining GOR V and Fragment Database Mining. Protein Science 2006, 15:2499-2506.
• [59]Cole C, Barber J, Barton G: The Jpred3 secondary structure prediction server. Nucleic Acids Research 2008, 36:W197-W202.
• [60]Blom N, Gammeltoft S, Brunak S: Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. Journal of Molecular Biology 1999, 294:1351-1362.
• [61]Puntervoll P, Linding R, Gemund C, Chabanis-Davidson S, Mattingsdal M, Cameron S, Martin DMA, Ausiello G, Brannetti B, Costantini A, et al.: ELM server: a new resource for investigating short functional sites in modular eukaryotic proteins. Nucleic Acids Research 2003, 31:3625-3630.
• [62]Martin NH, Willis JH: Ecological divergence associated with mating system causes nearly complete reproductive isolation between sympatric Mimulus species. Evolution 2007.
• [63]Ramsey J, Bradshaw HD Jr, Schemske DW: Components of reproductive isolation between the monkey flowers Mimulus lewishii and M. cardinalis (Phrymaceae). Evolution 2003, 57:1520-1534.