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Polymorphism of Sooty-fronted Spinetail (Synallaxis frontalis Aves: Furnariidae): Evidence of chromosomal rearrangements by pericentric inversion in autosomal macrochromosomes

Abstract

The Passeriformes is the most diverse and cytogenetically well-known clade of birds, comprising approximately 5,000 species. The sooty-fronted spinetail (Synallaxis frontalis Aves: Furnariidae) species, which belongs to the order Passeriformes, is typically found in South America, where it is widely distributed. Polymorphisms provide genetic variability, important for several evolutionary processes, including speciation and adaptation to the environment. The aim of this work was to analyze the possible cytotypes and systemic events involved in the species polymorphism. Of the sampled 19 individuals, two thirds were polymorphic, an event supposedly linked to mutations resulting from genomic evolution that can be transmitted hereditarily. A chromosomal polymorphism was detected between the 1st and 3rdpairs of autosomal macrochromosomes. This type of polymorphism is related to a pericentric inversion in regions involving chromosomal rearrangements. Differently from other polymorphism studies that report a link between polymorphic chromosomes and phenotypic changes, S. frontalis did not present any morphological variation in the sampled individuals.

Keywords:
Chromosomal polymorphism; evolution; cytogenetics

Introduction

The order Passeriformes comprises approximately 5,000 species and is the most diverse order within the class Aves. Few studies have demonstrated morphological variations, called polymorphism, in karyotypes of the same species. Polymorphism can be considered a gene marking mechanism, since they are hereditarily transmitted from the progenitor to the offspring, when viable (Balasubramanian et al., 2004Balasubramanian SP, Cox A, Brown NJ and Reed MW (2004) Candidate gene polymorphisms in solid cancers. Eur J Surg Oncol 30:593-601.). Among all Passeriformes karyotypes described so far, only five species presented chromosomal polymorphism (Thorneycroft, 1966Thorneycroft HB (1966) Chromosomal polymorphism in the White-throated Sparrow, Zonotrichia albicollis (Gmelin). Science 154:1571-1572.; Shields 1973Shields FG (1973) Chromosomal polymorphism common to several species of Junco (Aves). Can J Genet Cytol 15:461-471., 1976Shields FG (1976) Meiotic evidence for pericentric inversion polymorphism in Junco (Aves). Can J Genet Cytol 18:747-751.; Thomas et al., 2008Thomas JW, Cáceres M, Lowman JJ, Morehouse CB, Short ME, Baldwin EL, Maney DL and Martin CL (2008) The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement and suppressor of recombination. Genetics 179:1455-1468.; Itoh et al., 2011Itoh Y, Kampf K, Balakrishnan CN and Arnold AP (2011) Karyotypic polymorphism of the zebra finch Z chromosome. Chromosoma 120:255-264.; Kretschmer et al., 2018Kretschmer R, Lima VLC, de Souza MS, Costa AL, O’Brien PCM, Furguson-Smith MA, de Oliveira EHC, Gunski RJ and Garnero ADV (2018) Multidirectional chromosome painting in Synallaxis frontalis (Passeriformes, Furnariidae) reveals high chromosomal reorganization, involving fissions and inversions. Comp Cytogenet 12:97-110.)

Breakpoints are regions that accumulate hot spots that are being used and reused during genomic evolution (Glover and Stein, 1988Glover TW and Stein CK (1988) Chromosome breakage and recombination at fragile sites. Am J Hum Genet 43:265-273.). The fragile sites are evolutionary breakpoints, highly conserved and transmitted from a common ancestor (Ruiz-Herrera and Robinson, 2007Ruiz-Herrera A and Robinson TJ (2007) Afrotherian fragile sites, evolutionary breakpoints and phylogenetic inference from genomic assemblies. BMC Evol Biol 7:199.; Brown and O’Neill, 2010Brown JD and O’Neill RJ (2010) Chromosomes, conflict, and epigenetics: Chromosomal speciation revisited. Annu Rev Genomics Hum Genet 11:291-316.).

Olsson et al. (2001)Olsson ML, Irshaid NM, Hosseini-Maaf B, Hellberg A, Moulds MK and Sareneva H (2001) Genomic analysis of clinical samples with serologic ABO blood grouping discrepancies: Identification of 15 novel A and B subgroup alleles. Blood 98:1585-1593. believe that polymorphisms are responsible, in part, for genetic diversity, once they result in different phenotypes. The first chromosomal polymorphism described in birds was reported in Zonotrichia albicollis (Gmelin, 1789), and it is likely due to pericentric inversions in the second and third pairs of chromosomes (Thorneycroft, 1966Thorneycroft HB (1966) Chromosomal polymorphism in the White-throated Sparrow, Zonotrichia albicollis (Gmelin). Science 154:1571-1572.). In recent studies with this species, Thomas et al. (2008)Thomas JW, Cáceres M, Lowman JJ, Morehouse CB, Short ME, Baldwin EL, Maney DL and Martin CL (2008) The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement and suppressor of recombination. Genetics 179:1455-1468. discuss the relationship of this polymorphism with divergences in plumage and social behavior.

Shields (1973Shields FG (1973) Chromosomal polymorphism common to several species of Junco (Aves). Can J Genet Cytol 15:461-471., 1976Shields FG (1976) Meiotic evidence for pericentric inversion polymorphism in Junco (Aves). Can J Genet Cytol 18:747-751.) observed in Junco hyemalis (Linnaeus, 1758) a pericentric inversion involving the second and fifth chromosome pairs, but this variation was never seen simultaneously in the same karyotype. No significant change was found in the polymorphic individuals (physical or behavioral). The same results were described by Manolache (1974)Manolache M (1974) Chromosome polymorphism in the quail (Coturnix coturnix coturnix). Avian Chrom News 3:10. in Coturnix coturnix coturnix (Linnaeus, 1758), who demonstrated morphological differences in the second pair of autosomal chromosomes. Chromosomal translocation involving a chromosome in the third pair in Oriolus xanthornus (Horsfield, 1821) was reported as an important polymorphism, but it did not cause changes in the phenotype (Ansari and Kaul, 1978Ansari HA and Kaul D (1978) Translocation heterozigosity in the bird Lonchura punctulata (Linn.) (Ploceidae: Aves). Nat Acad Sci Lett 1:83-85.).

Genetic variability is fundamental for basic processes of natural selection; it occurs at individual levels and may or may not improve individual fitness. This mechanism occurs due to chromosomal changes, derived from translocations, inversions, mutations, deletions, and duplications in specific regions of the genome (Kageyama and Jacob, 1980Kageyama PY and Jacob WS (1980) Variação genética entre e dentro de populações de Araucaria Augustifolia (Bert) O. Ktze. In: I Encontro da IUFRO, Curitiba, pp. 83-86.; Nascimento et al., 1990Nascimento JÁ, Carvalho FIF and Barbosa NJF (1990) Agentes mutagênicos e a intensidade de variabilidade genética em caracteres adaptativos na cultura de aveia (Avena sativa L.). Agron Sulriograndense 26:199-216.).

The Furnariidae family belongs to the order Passeriformes, and it is currently composed of about 236 described species distributed into 71 genera, most of them endemic to South America and distributed in several ecological niches. Among the Furnariidae family, the genus Synallaxis is the most diverse, presenting 33 described species (Derryberry et al., 2011Derryberry EP, Claramunt S, Derryberry G, Chesser RT, Cracraft J, Aleixo A, Pérez-Emán J, Remsen Jr JV and Brumfield RT (2011) Lineage diversification and morphological evolution in a large-scale continental radiation: the neotropical ovenbirds and woodcreepers (Aves: Furnariidae). Evolution 65:2973-2986.; Sigrist, 2013)Sigrist T (2013) Guia de Campo Avis Brasilis - Avifauna Brasileira. 3rd edition. Avisbrasilis, São Paulo, 592 pp.. Despite this diversity, cytogenetic data are available for only five species: Furnarius rufus Gmelin, 1788, Lochmias nematura Lichtenstein, 1823 (Lucca and Rocha, 1992), Sittasomus griseicapillus Vieillot, 1818, and Lepidocolaptes angustirostris Vieillot, 1818 (Barbosa et al., 2013Barbosa MO, Silva RR, Correia VCS, Santos LP, Garnero AV and Gunski RJ (2013) Nucleolar organizer regions in Sittasomus griseicapillus and Lepidocolaptes angustirostris (Aves, Dendrocolaptidae): Evidence of a chromosome inversion. Genet Mol Biol 36:70-73.).

All karyotyped Furnariidae species have the same diploid number (2n=82) and show remarkable similarity in the chromosomal morphology, presenting few variations only in machrocromosomes, which are predominantly telocentric and acrocentric. Nevertheless, Synallaxis frontalis (Pelzeln, 1859) individuals present a striking characteristic of rearrangements that are responsible for small morphological variations in the chromosomal arms (Kretschmer et al., 2018Kretschmer R, Lima VLC, de Souza MS, Costa AL, O’Brien PCM, Furguson-Smith MA, de Oliveira EHC, Gunski RJ and Garnero ADV (2018) Multidirectional chromosome painting in Synallaxis frontalis (Passeriformes, Furnariidae) reveals high chromosomal reorganization, involving fissions and inversions. Comp Cytogenet 12:97-110.).

The chromosomal variations observed suggest a high chromosomal fragility, responsible for facilitating the occurrence of intraspecific chromosomal polymorphism. However, chromosomal polymorphism in individuals of a population may alter the karyotype pattern of these specimens (Teodoro-Pardo, 2007Teodoro-Pardo CVD (2007) Polimorfismo cromossômico en Capsicum annuum L. (Solanaceae) em recolectas de Puebla, Morelos y Quartenário, México. Agrociencia 41:873-881.).

Due to the chromosomal morphological variability in Synallaxis frontalis, this study aimed to analyze the possible karyotypes and systemic mechanisms involved in the polymorphism.

Materials and Methods

Nineteen specimens of Synallaxis frontalis (10 males and 9 females) were collected in the municipality of São Gabriel, RS, under the SISBIO licenses nº 44173-1 and nº 33860-1, and CEUA/UNIPAMPA, under protocol no. 026/2012. Captures occurred from 2013 to 2017, using a mist net. We also analyzed a family composed of a couple and four offspring (2 males and 2 females), called SFR family in this paper. The four individuals were captured in a non-random manner from the same nest.

Tissue cultures and chromosome preparation

Metaphases were obtained using short term culture of bone marrow (Garnero and Gunski, 2000Garnero AV and Gunski RJ (2000) Comparative analysis of the karyotypes of Nothura maculosa and Rynchotus rufescens (Aves: Tinamidae): A case of chromosomal polymorphism. Nucleus 43:64–70.) and fibroblast from biopsies, according to the Sasaki et al. (1968)Sasaki M, Ikeuchi T and Maino S (1968) A feather pulp culture for avian chromosomes with notes on the chromosomes of the peafowl and the ostrich. Experientia 24:1923–1929. method with modifications, in which samples were fractionated mechanically and incubated in collagenase solution (0.0186 g in 4 mL of DMEM medium), for 1 h at 37 °C for cell dissociation. After centrifugation and discarding the supernatant, 5 mL of DMEM supplemented with antibiotics and fetal bovine serum (15%) were added, and the material was transferred to cell culture flasks. Both methods included colcemid incubation, hypotonic treatment, and fixation with methanol:acetic acid (3:1).

Conventional cytogenetics: Giemsa staining, C-banding, G-banding and karyotyping

The distribution of heterochromatic blocks was analyzed by C-banding (Ledesma et al., 2006Ledesma MA, Martinez PA, Calderón OS, Boeris JM and Meriles JM (2006) Descrição do cariótipo e padrões de bandas C e NOR em Pheucticus aureoventris (Emberizidae: Cardinalinae). Rev Bras Ornitol 14:5962.), with modifications. After incubation at 60 °C for 1 h, the slides were treated with 0.2 N HCl for 10 min, 50% Ba (OH2) for 15 min at 37 °C, 0.01 N HCl for 2 min, 2 SSC at 60 °C for 1h and 30 min, and stained with Giemsa (5% in 0.07M phosphate buffer, pH 6.8) for 15 min. Karyotypes were arranged according to Levan et al. (1964)Levan A, Fredga K and Samdberg AR (1964) Nomenclature for centromerlc position on chromosomes. Hereditas 52:201-220., and the chromosomes were classified as metacentric, submetacentric, subtelocentric, and telocentric according to arm ratio (r) and centromeric index (i). The G-band analysis and patterns were done according to Howe et al. (2014)Howe B, Umrigar A and Tsien F (2014) Chromosome preparation from cultured cells. J Vis Exp 83:e50203..

Microscopic analysis

We analyzed approximately 30 metaphase spreads per individual in an optical microscope (OLYMPUS DP53) to confirm chromosome number and morphology. For composing karyotype figures, Corel Draw® 12 was used.

Results

Synallaxis frontalis presented the diploid number of 82 chromosomes, with 11 pairs of macrochromosomes, including sex chromosomes Z and W, and 30 pairs of microchromosomes (Figure 1A-C). Of all the cytotypes analyzed in this study, the second, fifth, sixth and seventh pairs presented a subtelocentric morphology. Differently, the fourth pair was submetacentric, the eighth pair and the sex chromosomes were metacentric, and the remaining others were telocentric.

Figure 1
Classical cytogenetics techniques in Synallaxis frontalis (SFR). (A) Conventional staining of metaphases from a male; arrows indicate the sexual chromosome Z. (B) Partial karyotype containing macrochromosomes, microchromosomes, and sex chromosomes. (C). C-banding of a female showing the W sex chromosome, entirely heterochromatic. (D) Five distinct cytotypes found in samples.

We found a chromosomal polymorphism originated from a break followed by a pericentric inversion in the first and third autosomal pairs. Five different cytotypes were observed, these being the standard telocrocentric in the 1st pair and a subtelocentric in the 3rd (Table 1). All the cytotypes found in S. frontalis are described in Figure 1D.

Table 1
Cytotype frequency in Synallaxis frontalis.

The C-banding analyses showed blocks of constitutive heterochromatin in the centromeric regions of some of the macrochromosomes and microchromosomes. The sex chromosome W was entirely heterochromatic (Figure 1C).

The G-banding pattern in S. frontalis had evidence of pericentromeric inversions in the heteromorphic chromosomes. The inversions involved one positive band, two negative bands, and the centromere in the first and third pairs (Figure 2).

Figure 2
G-banding patterns found in standard and polymorphic individuals. Metaphasis of a standard (A) and polymorphic (B) bird; arrows indicate the first chromosome pair expanded in the box. (C) Schematic illustration of pericentric inversion.

Among the 19 sampled individuals, two thirds presented polymorphisms in the first, third, or in both pairs; generally, the frequency of polymorphic individuals was higher than that of non-polymorphic ones in both sexes. Heterozygous individuals were more abundant in polymorphism than polymorphic homozygotes or standard ones.

Two cytotypes were found in the SFR family. Females presented a heterozygous polymorphism in the third pair, while the males presented a standard cytotype (Figure 3).

Figure 3
Heredogram of the SFR family. Circles represent the females and squares, the males. The numbers refer to chromosome pairs. t: telocentric; st: subtelocentric; sm: submetacentric.

Discussion

The diploid and chromosomal morphologies found in the sampled birds were similar to those of Furnariidae species (chromosome number around 80), as described in the literature (Barbosa et al., 2013Barbosa MO, Silva RR, Correia VCS, Santos LP, Garnero AV and Gunski RJ (2013) Nucleolar organizer regions in Sittasomus griseicapillus and Lepidocolaptes angustirostris (Aves, Dendrocolaptidae): Evidence of a chromosome inversion. Genet Mol Biol 36:70-73.). It is known that the first and third chromosome pairs are heteromorphic in this species, and we found in some individuals short arms of different lengths in pairs 1 and 3 (Figure 1) (Kretschmer et al., 2018Kretschmer R, Lima VLC, de Souza MS, Costa AL, O’Brien PCM, Furguson-Smith MA, de Oliveira EHC, Gunski RJ and Garnero ADV (2018) Multidirectional chromosome painting in Synallaxis frontalis (Passeriformes, Furnariidae) reveals high chromosomal reorganization, involving fissions and inversions. Comp Cytogenet 12:97-110.).

One in three analyzed birds presented the standard karyotype, and the other two had karyotypes varying within four different cytotypes. The frequency of polymorphism was very high. However, a reasonable portion of individuals had a standard cytotype. This cytotype was thus defined based on cytogenetic and phylogenetic data. The phylogeny of the Furnariidae family defines the genus Synallaxis as slightly derived within the group (Irestedt et al., 2009Irestedt M, Fjeldsa J, Dalén L and Ericson PG (2009) Convergent evolution, habitat shifts and variable diversification rates in the ovenbird-woodcreeper family (Furnariidae). BMC Evol Biol 9:268-270.).

In a recent work, the morphological variations in chromosome pairs 1 and 3 were defined as heteromorphism, since it would be necessary to analyze a larger sample to define them as polymorphism (Kretschmer et al., 2018Kretschmer R, Lima VLC, de Souza MS, Costa AL, O’Brien PCM, Furguson-Smith MA, de Oliveira EHC, Gunski RJ and Garnero ADV (2018) Multidirectional chromosome painting in Synallaxis frontalis (Passeriformes, Furnariidae) reveals high chromosomal reorganization, involving fissions and inversions. Comp Cytogenet 12:97-110.). Nevertheless, our study showed that variations in morphology are polymorphisms by the distribution and fixation of different cytotypes in the specimens sampled.

From the 19 analyzed birds, 12 presented some of the described polymorphic cytotypes (Table 1). The most common polymorphic cytotype (36% approximately) was the heterozygous polymorphism in the third chromosomal pair. Less common cytotypes observed were heterozygous polymorphisms for both chromosome pairs and homozygous polymorphisms for any of the pairs. This data together with the karyotype analysis of the species emphasizes the possibility that there are no pre- or post-zygotic barriers to any of the possible polymorphic combinations in S. frontalis (Figure 1).

According to Kretschmer et al. (2018)Kretschmer R, Lima VLC, de Souza MS, Costa AL, O’Brien PCM, Furguson-Smith MA, de Oliveira EHC, Gunski RJ and Garnero ADV (2018) Multidirectional chromosome painting in Synallaxis frontalis (Passeriformes, Furnariidae) reveals high chromosomal reorganization, involving fissions and inversions. Comp Cytogenet 12:97-110., hybridization with Leucopternis albicollis (LAL) probes has revealed the possible mechanism responsible for its specific morphological variation, assuming that both polymorphisms would have arisen either by pericentric inversions or centromere repositioning. Indeed, our study has shown through G-banding that the origin of the polymorphic chromosomal pairs comes from pericentric inversions, where the bands 1, 2 and 3 of the q-arm of a single chromosome in pair 1 became bands 1, 2 and 3 of the p-arm (Figure 2C). This inversion includes the centromere, discarding the possibility of centromere repositioning. The same also occurred in the third chromosomal pair of this species.

Genetic changes related to the S. frontalis polymorphism could be favorable for this species, as indicated by the high frequency of polymorphic individuals found in this study. However, further studies are needed to confirm this. Such mechanisms are associated with evolutionary phases and events of speciation, as reported in Frankham et al. (2002)Frankham R, Ballou JD and Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge, 630 pp..

A polymorphism is inherited when there is no pre- or post-zygotic barrier (Balasubramanian et al., 2004Balasubramanian SP, Cox A, Brown NJ and Reed MW (2004) Candidate gene polymorphisms in solid cancers. Eur J Surg Oncol 30:593-601.). Based on the SFR family analysis, we can infer that there is no pre-zygotic barrier, because the progenitors presented the polymorphic, as well as the standard cytotypes. Furthermore, the offspring showed two chromosomal morphotypes, confirming that the polymorphism is inheritable. Also, we highlight that the polymorphism mechanism in S. frontalis is not related to sex.

However, it is difficult to determine the size or the number of populations of this species because it is widely distributed in South America, and it is unlikely that there are possible genetic or geographical barriers separating populations.

It is assumed that the presence of breakpoints or hot spots in the chromosomal regions of this species are inversions. This could be considered an advantageous evolutionary characteristic for S. frontalis; however, it is not possible to estimate or argue that speciation occurred in the specimens analyzed. During genomic evolution of a species, the accumulation of breakpoints is frequent (Glover and Stein, 1988Glover TW and Stein CK (1988) Chromosome breakage and recombination at fragile sites. Am J Hum Genet 43:265-273.). The inversions found in the polymorphic individuals of this study demonstrate how important this system is for the genetic variability and maintenance of mechanisms that originate the polymorphism within the population.

In S. frontalis there is no apparent phenotypic characteristic that differentiates individuals as polymorphisms (Thorneycroft, 1966Thorneycroft HB (1966) Chromosomal polymorphism in the White-throated Sparrow, Zonotrichia albicollis (Gmelin). Science 154:1571-1572.; Thomas et al., 2008Thomas JW, Cáceres M, Lowman JJ, Morehouse CB, Short ME, Baldwin EL, Maney DL and Martin CL (2008) The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement and suppressor of recombination. Genetics 179:1455-1468.). In contrast, Zonotrichia albicollis has a polymorphism that causes changes in behavior and plumage. Thus, as also seen in the SFR family, one can conclude that there is no visible sexual or environmental selection of polymorphic or non-polymorphic individuals living in sympatry.

In conclusion, the present work indicates that there is striking diversity in S. frontallis karyotype composition, leading to several cytotypes. This variability may be the result of evolutionary processes. The study of such species can contribute to the understanding of how phylogenetic diversity occurs, and thus the preservation and further study of this species is important.

Acknowledgments

Authors would like to thank all colleagues from our laboratory (Grupo de Pesquisa Diversidade Genética Animal). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

Conflict of interest

The authors declare that there is no conflict of interest that could be perceived as prejudicial to the impartiality of the reported research.

Author contributions

MSS, SAB and ALC conceived and designed the study; MSS, SAB, ALC and RJG conducted the experiments; MSS, SAB, ALC, RK, AVG and RJG analyzed the data; MSS, SAB and ALC wrote the manuscript; AVG and RJG supervision, all authors read and approved the final version.

References

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  • Balasubramanian SP, Cox A, Brown NJ and Reed MW (2004) Candidate gene polymorphisms in solid cancers. Eur J Surg Oncol 30:593-601.
  • Barbosa MO, Silva RR, Correia VCS, Santos LP, Garnero AV and Gunski RJ (2013) Nucleolar organizer regions in Sittasomus griseicapillus and Lepidocolaptes angustirostris (Aves, Dendrocolaptidae): Evidence of a chromosome inversion. Genet Mol Biol 36:70-73.
  • Brown JD and O’Neill RJ (2010) Chromosomes, conflict, and epigenetics: Chromosomal speciation revisited. Annu Rev Genomics Hum Genet 11:291-316.
  • Derryberry EP, Claramunt S, Derryberry G, Chesser RT, Cracraft J, Aleixo A, Pérez-Emán J, Remsen Jr JV and Brumfield RT (2011) Lineage diversification and morphological evolution in a large-scale continental radiation: the neotropical ovenbirds and woodcreepers (Aves: Furnariidae). Evolution 65:2973-2986.
  • Frankham R, Ballou JD and Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge, 630 pp.
  • Garnero AV and Gunski RJ (2000) Comparative analysis of the karyotypes of Nothura maculosa and Rynchotus rufescens (Aves: Tinamidae): A case of chromosomal polymorphism. Nucleus 43:64–70.
  • Glover TW and Stein CK (1988) Chromosome breakage and recombination at fragile sites. Am J Hum Genet 43:265-273.
  • Howe B, Umrigar A and Tsien F (2014) Chromosome preparation from cultured cells. J Vis Exp 83:e50203.
  • Irestedt M, Fjeldsa J, Dalén L and Ericson PG (2009) Convergent evolution, habitat shifts and variable diversification rates in the ovenbird-woodcreeper family (Furnariidae). BMC Evol Biol 9:268-270.
  • Itoh Y, Kampf K, Balakrishnan CN and Arnold AP (2011) Karyotypic polymorphism of the zebra finch Z chromosome. Chromosoma 120:255-264.
  • Kageyama PY and Jacob WS (1980) Variação genética entre e dentro de populações de Araucaria Augustifolia (Bert) O. Ktze. In: I Encontro da IUFRO, Curitiba, pp. 83-86.
  • Kretschmer R, Lima VLC, de Souza MS, Costa AL, O’Brien PCM, Furguson-Smith MA, de Oliveira EHC, Gunski RJ and Garnero ADV (2018) Multidirectional chromosome painting in Synallaxis frontalis (Passeriformes, Furnariidae) reveals high chromosomal reorganization, involving fissions and inversions. Comp Cytogenet 12:97-110.
  • Ledesma MA, Martinez PA, Calderón OS, Boeris JM and Meriles JM (2006) Descrição do cariótipo e padrões de bandas C e NOR em Pheucticus aureoventris (Emberizidae: Cardinalinae). Rev Bras Ornitol 14:5962.
  • Levan A, Fredga K and Samdberg AR (1964) Nomenclature for centromerlc position on chromosomes. Hereditas 52:201-220.
  • Manolache M (1974) Chromosome polymorphism in the quail (Coturnix coturnix coturnix). Avian Chrom News 3:10.
  • Nascimento JÁ, Carvalho FIF and Barbosa NJF (1990) Agentes mutagênicos e a intensidade de variabilidade genética em caracteres adaptativos na cultura de aveia (Avena sativa L.). Agron Sulriograndense 26:199-216.
  • Olsson ML, Irshaid NM, Hosseini-Maaf B, Hellberg A, Moulds MK and Sareneva H (2001) Genomic analysis of clinical samples with serologic ABO blood grouping discrepancies: Identification of 15 novel A and B subgroup alleles. Blood 98:1585-1593.
  • Ruiz-Herrera A and Robinson TJ (2007) Afrotherian fragile sites, evolutionary breakpoints and phylogenetic inference from genomic assemblies. BMC Evol Biol 7:199.
  • Sasaki M, Ikeuchi T and Maino S (1968) A feather pulp culture for avian chromosomes with notes on the chromosomes of the peafowl and the ostrich. Experientia 24:1923–1929.
  • Shields FG (1973) Chromosomal polymorphism common to several species of Junco (Aves). Can J Genet Cytol 15:461-471.
  • Shields FG (1976) Meiotic evidence for pericentric inversion polymorphism in Junco (Aves). Can J Genet Cytol 18:747-751.
  • Sigrist T (2013) Guia de Campo Avis Brasilis - Avifauna Brasileira. 3rd edition. Avisbrasilis, São Paulo, 592 pp.
  • Teodoro-Pardo CVD (2007) Polimorfismo cromossômico en Capsicum annuum L. (Solanaceae) em recolectas de Puebla, Morelos y Quartenário, México. Agrociencia 41:873-881.
  • Thomas JW, Cáceres M, Lowman JJ, Morehouse CB, Short ME, Baldwin EL, Maney DL and Martin CL (2008) The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement and suppressor of recombination. Genetics 179:1455-1468.
  • Thorneycroft HB (1966) Chromosomal polymorphism in the White-throated Sparrow, Zonotrichia albicollis (Gmelin). Science 154:1571-1572.
  • Associate Editor: Yatiyo Yonenaga-Yassuda

Publication Dates

  • Publication in this collection
    11 Mar 2019
  • Date of issue
    Jan-Mar 2019

History

  • Received
    21 Feb 2018
  • Accepted
    26 June 2018
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