Studies on mammals demonstrate wide interspecific variation in the number and distribution of recombination events along chromosomes. Birds represent an interesting model group for comparative analysis of cytological and ecological drivers of recombination rate evolution. Yet, data on variation in recombination rates in birds are limited to a dozen of species. In this study, we used immunolocalization of MLH1, a mismatch repair protein marking mature recombination nodules, to estimate the overall recombination rate and distribution of crossovers along macrochromosomes in female and male meiosis of the gray goose (Anser anser). The average number of MLH1 foci was significantly higher in oocytes than in spermatocytes (73.6 ± 7.8 and 58.9 ± 7.6, respectively). MLH1 foci distribution along individual macrobivalents showed subtelomeric peaks, which were more pronounced in males. Analysis of distances between neighboring MLH1 foci on macrobivalents revealed stronger crossover interference in male meiosis. These data create a framework for future genetic and physical mapping of the gray goose.

1.
Akesson M, Hansson B, Hasselquist D, Bensch S: Linkage mapping of AFLP markers in a wild population of great reed warblers: importance of heterozygosity and number of genotyped individuals. Mol Ecol 16:2189-2202 (2007).
2.
Anderson LK, Reeves A, Webb L, Ashley T: Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151:1569-1579 (1999).
3.
Anderson LK, Salameh N, Bass HW, Harper LC, Cande WZ, et al: Integrating genetic linkage maps with pachytene chromosome structure in maize. Genetics 166:1923-1933 (2004).
4.
Andraszek K, Smalec E: Avian meiotic chromosomes as model objects in cytogenetics, in Swan A (ed): Meiosis. Molecular Mechanisms and Cytogenetic Diversity, pp 123-148 (InTech, Rijeka 2012).
5.
Andraszek K, Wojcik E, Grużewska A, Smalec E: Genome size of the European domestic goose (Anser anser domesticus). Can J Anim Sci 89:449-455 (2009).
6.
Aslam ML, Bastiaansen JW, Crooijmans RP, Vereijken A, Megens HJ, Groenen MA: A SNP based linkage map of the turkey genome reveals multiple intrachromosomal rearrangements between the turkey and chicken genomes. BMC Genomics 11:647 (2010).
7.
Backström N, Brandström M, Gustafsson L, Qvarnström A, Cheng H, Ellegren H: Genetic mapping in a natural population of collared flycatchers (Ficedula albicollis): conserved synteny but gene order rearrangements on the avian Z chromosome. Genetics 174:377-386 (2006).
8.
Backström N, Karaiskou N, Leder EH, Gustafsson L, Primmer CR, et al: A gene-based genetic linkage map of the collared flycatcher (Ficedula albicollis) reveals extensive synteny and gene-order conservation during 100 million years of avian evolution. Genetics 179:1479-1495 (2008).
9.
Backström N, Forstmeier W, Schielzeth H, Mellenius H, Nam K, et al: The recombination landscape of the zebra finch Taeniopygia guttata genome. Genome Res 20:485-495 (2010).
10.
Baker SM, Plug AW, Prolla TA, Bronner CE, Harris AC, et al: Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat Genet 13:336-342 (1996).
11.
Basheva EA, Bidau CJ, Borodin PM: General pattern of meiotic recombination in male dogs estimated by MLH1 and RAD51 immunolocalization. Chromosome Res 16:709-719 (2008).
12.
Basheva EA, Torgasheva AA, Sakaeva GR, Bidau C, Borodin PM: A- and B-chromosome pairing and recombination in male meiosis of the silver fox (Vulpes vulpes L., 1758, Carnivora, Canidae). Chromosome Res 18:689-696 (2010).
13.
Berchowitz LE, Copenhaver GP: Genetic interference: don't stand so close to me. Curr Genomics 11:91-102 (2010).
14.
Borodin PM, Karamysheva TV, Belonogova NM, Torgasheva AA, Rubtsov NB, Searle JB: Recombination map of the common shrew, Sorex araneus (Eulipotyphla, Mammalia). Genetics 178:621-632 (2008).
15.
Borodin PM, Basheva EA, Zhelezova AI: Immunocytological analysis of meiotic recombination in the American mink (Mustela vison). Anim Genet 40:235-238 (2009).
16.
Burt A, Bell G: Mammalian chiasma frequencies as a test of two theories of recombination. Nature 326:803-805 (1987).
17.
Calderón PL, Pigozzi MI: MLH1-focus mapping in birds shows equal recombination between sexes and diversity of crossover patterns. Chromosome Res 14:605-612 (2006).
18.
Chang SB, Anderson LK, Sherman JB, Royer SM, Stack SM: Predicting and testing physical locations of genetically mapped loci on tomato pachytene chromosome 1. Genetics 176:2131-2138 (2007).
19.
Christidis L: Aves, in John B (ed): Animal Cytogenetics, vol 4 (Gebrüder Bornträger, Berlin 1990).
20.
Dumont BL, Payseur BA: Evolution of the genomic rate of recombination in mammals. Evolution 62:276-294 (2008).
21.
Dumont BL, Payseur BA: Evolution of the genomic recombination rate in murid rodents. Genetics 187:643-657 (2011a).
22.
Dumont BL, Payseur BA: Genetic analysis of genome-scale recombination rate evolution in house mice. PLoS Genet 7:e1002116 (2011b).
23.
Dumont BL, White MA, Steffy B, Wiltshire T, Payseur BA: Extensive recombination rate variation in the house mouse species complex inferred from genetic linkage maps. Genome Res 21:114-125 (2011).
24.
Ellegren H: Evolutionary stasis: the stable chromosomes of birds. Trends Ecol Evol 25:283-291 (2010).
25.
Falque M, Anderson LK, Stack SM, Gauthier F, Martin OC: Two types of meiotic crossovers coexist in maize. Plant Cell 21:3915-3925 (2009).
26.
Froenicke L, Anderson LK, Wienberg J, Ashley T: Male mouse recombination maps for each autosome identified by chromosome painting. Am J Hum Genet 71:1353-1368 (2002).
27.
Gauthier F, Martin OC, Falque M: CODA (crossover distribution analyzer): quantitative characterization of crossover position patterns along chromosomes. BMC Bioinformatics 12:27 (2011).
28.
Gregory TR: Genome size evolution in animals, in Gregory TR (ed): The Evolution of the Genome, pp 4-87 (Elsevier, New York 2005).
29.
Gregory TR: Animal Genome Size Database (2016). http://www.genomesize.com.
30.
Griffin DK, Robertson LB, Tempest HG, Skinner BM: The evolution of the avian genome as revealed by comparative molecular cytogenetics. Cytogenet Genome Res 117:64-77 (2007).
31.
Groenen MA, Wahlberg P, Foglio M, Cheng HH, Megens HJ, et al: A high-density SNP-based linkage map of the chicken genome reveals sequence features correlated with recombination rate. Genome Res 19:510-519 (2009).
32.
Haldane J: Sex ratio and unisexual sterility in hybrid animals. J Genet 12:101-109 (1922).
33.
Hansson B, Akesson M, Slate J, Pemberton JM: Linkage mapping reveals sex-dimorphic map distances in a passerine bird. Proc Biol Sci 272:2289-2298 (2005).
34.
Hansson B, Ljungqvist M, Dawson DA, Mueller JC, Olano-Marin J, et al: Avian genome evolution: insights from a linkage map of the blue tit (Cyanistes caeruleus). Heredity (Edinb) 104:67-78 (2010).
35.
Hassold T, Sherman S, Hunt P: Counting cross-overs: characterizing meiotic recombination in mammals. Hum Mol Genet 9:2409-2419 (2000).
36.
Hassold T, Hansen T, Hunt P, VandeVoort C: Cytological studies of recombination in rhesus males. Cytogenet Genome Res 124:132-138 (2009).
37.
Hughes AL: Adaptive Evolution of Genes and Genomes (Oxford University Press, New York 1999).
38.
Huxley J: Sexual difference of linkage in Gammarus chevreuxi. J Genet 20:145-156 (1928).
39.
Jaari S, Li MH, Merila J: A first-generation microsatellite-based genetic linkage map of the Siberian jay (Perisoreus infaustus): insights into avian genome evolution. BMC Genomics 10:1 (2009).
40.
Kawakami T, Smeds L, Backström N, Husby A, Qvarnström A, et al: A high-density linkage map enables a second-generation collared flycatcher genome assembly and reveals the patterns of avian recombination rate variation and chromosomal evolution. Mol Ecol 23:4035-4058 (2014).
41.
Kleckner N, Storlazzi A, Zickler D: Coordinate variation in meiotic pachytene SC length and total crossover/chiasma frequency under conditions of constant DNA length. Trends Genet 19:623-628 (2003).
42.
Lu L, Chen Y, Wang Z, Li X, Chen W, et al: The goose genome sequence leads to insights into the evolution of waterfowl and susceptibility to fatty liver. Genome Biol 16:89 (2015).
43.
Lynn A, Koehler KE, Judis L, Chan ER, Cherry JP, et al: Covariation of synaptonemal complex length and mammalian meiotic exchange rates. Science 296:2222-2225 (2002).
44.
Masabanda JS, Burt DW, O'Brien PC, Vignal A, Fillon V, et al: Molecular cytogenetic definition of the chicken genome: the first complete avian karyotype. Genetics 166:1367-1373 (2004).
45.
Pardo-Manuel de Villena F, Sapienza C: Recombination is proportional to the number of chromosome arms in mammals. Mamm Genome 12:318-322 (2001).
46.
Peters AH, Plug AW, van Vugt MJ, Boer P de: A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosome Res 5:66-68 (1997).
47.
Peterson DG, Stack SM, Healy JL, Donohoe BS, Anderson LK: The relationship between synaptonemal complex length and genome size in four vertebrate classes (Osteicthyes, Reptilia, Aves, Mammalia). Chromosome Res 2:153-162 (1994).
48.
Pigozzi MI: Distribution of MLH1 foci on the synaptonemal complexes of chicken oocytes. Cytogenet Genome Res 95:129-133 (2001).
49.
Pigozzi MI, del Priore L: Meiotic recombination analysis in female ducks (Anas platyrhynchos). Genetica 144:307-312 (2016).
50.
Pigozzi MI, Solari AJ: Equal frequencies of recombination nodules in both sexes of the pigeon suggest a basic difference with eutherian mammals. Genome 42:315-321 (1999a).
51.
Pigozzi MI, Solari AJ: Recombination nodule mapping and chiasma distribution in spermatocytes of the pigeon, Columba livia. Genome 42:308-314 (1999b).
52.
Reeves A: MicroMeasure: a new computer program for the collection and analysis of cytogenetic data. Genome 44:439-443 (2001).
53.
Segura J, Ferretti L, Ramos-Onsins S, Capilla L, Farre M, et al: Evolution of recombination in eutherian mammals: insights into mechanisms that affect recombination rates and crossover interference. Proc Biol Sci 280:20131945 (2013).
54.
Shahin AA, Ata AT, Shnaf AS: Karyotype and C-banding pattern of the domestic geese Anser anser populations (Aves: Anatidae) in Egypt. Folia Biol (Krakow) 62:49-58 (2014).
55.
Smeds L, Mugal CF, Qvarnström A, Ellegren H: High-resolution mapping of crossover and non-crossover recombination events by whole-genome re-sequencing of an avian pedigree. PLoS Genet 12:e1006044 (2016).
56.
Solari AJ: Equalization of Z and W axes in chicken and quail oocytes. Cytogenet Cell Genet 59:52-56 (1992).
57.
Solari AJ, Pigozzi MI: Recombination nodules and axial equalization in the ZW pairs of the Peking duck and the guinea fowl. Cytogenet Cell Genet 64:268-272 (1993).
58.
Stapley J, Birkhead TR, Burke T, Slate J: A linkage map of the zebra finch Taeniopygia guttata provides new insights into avian genome evolution. Genetics 179:651-667 (2008).
59.
van Oers K, Santure AW, de Cauwer I, van Bers NE, Crooijmans RP, et al: Replicated high-density genetic maps of two great tit populations reveal fine-scale genomic departures from sex-equal recombination rates. Heredity (Edinb) 112:307-316 (2014).
60.
Zhou Q, Zhang J, Bachtrog D, An N, Huang Q, et al: Complex evolutionary trajectories of sex chromosomes across bird taxa. Science 346:1246338 (2014).
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.