Meiotic Analysis of Gomphidae Species Sheds Light on the Large X Chromosome of the Family (Anisoptera, Odonata)
1
Laboratorio de Citogenética y Evolución, Departamento de Ecología, Genética y Evolución, Instituto de Ecología, Genética y Evolución (CONICET-UBA), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160, Ciudad Autónoma de Buenos Aires C1428EGA, Argentina
2
Facultad de Bromatología, Universidad Nacional de Entre Ríos, Sede Centro. 25 de mayo 709, Gualeguaychú E2822ABA, Entre Ríos, Argentina
3
Instituto de Ecología, Genética y Evolución (CONICET-UBA), Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Güiraldes 2160, Ciudad Autónoma de Buenos Aires C1428EGA, Argentina
4
Independent Researcher, Ciudad Autónoma de Buenos Aires C1176ABM, Argentina
*
Author to whom correspondence should be addressed.
Diversity 2022, 14(10), 874; https://doi.org/10.3390/d14100874
Submission received: 3 August 2022
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Revised: 5 October 2022
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Accepted: 6 October 2022
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Published: 17 October 2022
(This article belongs to the Special Issue Diversity, Ecology and Evolution of Odonata)
Abstract
:In most Anisoptera families, the modal diploid number is 25 in males (24 autosomes + X), and the X chromosome is one of the smallest elements of the complement. The family Gomphidae is an exception, as it has a modal diploid number of 23 (22 + X), and the X chromosome is the largest of the complement and of medium-to-large size in many species. We studied the meiosis of three gomphid species from Argentina: Aphylla cf. distinguenda (Campion, 1920), Phyllocycla propinqua Belle, 1972 and Phyllocycla sp. Chromosome number is 2n = 23, n = 11 + X, except for Phyllocycla propinqua, showing n = 10 + X. The X chromosome of these species is medium-sized and presents heteropyknotic blocks of different sizes. Despite the small number of gomphid species analysed, there is a clear trend of increasing size of the X chromosome with the increasing amount of heterochromatin. Our results, together with those from the literature, suggest that its large size might have been due to a progressive accumulation of repetitive DNA and heterochromatinisation and not to fusion, as previously suggested. This led us to propose that the ancestral number coincided with the modal number of Gomphidae. A revision of the derived sex-determining systems in Odonata is also provided.
1. Introduction
Gomphidae is the second largest family of the suborder Anisoptera, with approximately 1000 species. Among the most species-rich genera, Aphylla, Phyllocycla, Phyllogomphoides and Progomphus are mainly distributed in the Neotropics but are also found in the Nearctic region [1].
Odonata exhibits some particular cytogenetic features, such as holokinetic chromosomes (i.e., without primary constriction or centromere) and equatorial division of the X chromosome, but the type of meiosis of autosomes is controversial. Some authors establish that meiosis is post-reductional (i.e., sister chromatids separate in the first division and homologues in the second one). They are based on the orientation of the bivalents with subterminal ciasmata on the equatorial plane, the equational division of the heteromorphic autosomal and neo-sex bivalents, and autosomal trivalents at metaphase I. These lead to the presence of heteromorphic chromatids or three chromatids, respectively, at all metaphases II [2]. Instead, Nokkala and collaborators [3] consider that the meiotic division of the autosomes is pre-reductional (canonical) based on the study of one species that presents only interstitial chiasmata and their interpretation of the migration of the homologous telomeres at anaphase I. Odonata is also characterised by having a single chiasma in all the bivalents and a noticeably small autosome pair (m-chromosomes) of about half the size of the following pair, which shows a regular meiotic behaviour [2].
The chromosome number has been determined in more than 600 species of the order belonging to 23 families [4]. In the Neotropical region, cytogenetic data have been reported for about 235 species from eight countries (Argentina, Bolivia, Brazil, Chile, Perú, Suriname, Uruguay and Venezuela) [4].
Although the haploid number is relatively constant (12, 13 or 14) in nearly 93% of the species, the chromosome number ranges from n = 3 in Macrothemis hemichlora (Burmeister, 1839) to n = 21 in Orthemis nodiplaga Karsch, 1891 (Libellulidae). In the families of the suborder Anisoptera, the modal haploid number is 12 in Gomphidae, 13 in Cordulegasteridae, Corduliidae, Libellulidae and Macrodiplacidae, and 14 in Aeshnidae [2,4,5,6].
About 95% of the species possess an XX/X0 sex-determination chromosome system with male heterogamety. The X chromosome is generally the smallest of the complement or the second smallest element after the m chromosomes. In contrast, it is the largest of the complement in some Gomphidae species and different theories have been postulated to explain its unusual size [7,8,9,10,11,12,13,14,15,16,17]. The sex chromosome systems may have originated from fusions or insertions, such as the neo-XY/neo-XX system and the multiple X1X2Y/X1X1X2X2 system in Micrathyria ungulata [2,4,6,11,18].
C-banding revealed that most autosomes have heterochromatic blocks in both telomeric regions, which are either small or large and symmetric or asymmetric [19]. The X chromosome of males is entirely C-positive, and exhibits intermediate staining or possesses C-positive bands localised in the terminal or interstitial regions [6,15,19,20,21,22,23,24].
In the present study, we analysed the meiotic behaviour and the characteristics of the X chromosome in three species of Gomphidae: Aphylla cf. distinguenda (Campion, 1920), Phyllocycla propinqua Belle, 1972 and Phyllocycla sp., and discuss the origin of the large X chromosomes and the diploid number of the common ancestor of Gomphidae. Moreover, we provide a review of the derived sex-determining systems in the order.
2. Material and Methods
The present study was conducted on three adult males of Aphylla cf. distinguenda and one adult male of Phyllocycla sp. from Tigre in the Lower Delta of the Paraná River (30°28′00″ S 62°49′59″ W) (Buenos Aires Province), and six adult males of Phyllocycla propinqua from Arroyo León, Department of Eldorado (26°24′04″ S 54°37′07″ W) (Misiones Province), Argentina. Administration of National Parks of Argentina issued the permit for the collection and transport of material in the protected area.
Within the cosmopolitan family Gomphidae, the genus Phyllocycla is distributed from southern Mexico to Uruguay and northern Argentina, and the genus Aphylla from southeast United States to Uruguay and northern Argentina [25].
The specimens were etherised in the field, their abdomen was longitudinally incised on the dorsal side and they were whole fixed in 3:1 (absolute ethanol: glacial acetic acid). Later, the gonads were dissected out and immersed in fresh fixative for 24 h before storage in 70% ethanol at 4 °C. For meiotic studies, a piece of gonad was placed in 45% acetic acid for 2 to 3 min to facilitate cell spreading and slides were made by the squash technique in iron propionic haematoxylin.
3. Results
Aphylla cf. distinguenda (2n = 23, n = 11 + X). At spermatogonial metaphase there are 23 chromosomes; the X chromosome is the largest of the complement and lies at the centre of an autosomal ring, where the distinguishable pairs of homologues appear to be close to each other (Figure 1A). During prophase I until diplotene, the large X chromosome shows a large positively heteropyknotic telomeric region, a slim subterminal isopycnotic region and a medium positively heteropyknotic telomeric region (Figure 1B,C). From diplotene onwards, bivalents have one chiasma in submedial or (less frequently) medial position and decrease gradually in size, except for the m bivalent, which is half the size of the lower bivalent; the size of the X chromosome is similar to that of the medium bivalents (Figure 1D). At prophase II, the autosomes adopt the typical epsilon ξ-like shape and the X chromosome is composed of a single chromatid (Figure 1E). At metaphase II, the X chromosome lies on the equatorial plate together with the autosomes (Figure 1F).
One of the individuals studied showed a variation in the chromosome number at the first and second meiotic divisions. Of 28 diplotenes and diakineses analysed, 23 cells presented 11 + X and 5 10 + X, whereas of 27 prometaphases and metaphases II, 2 presented 11 + X and 25 10 + X (Figure 1E,F).
Phyllocycla propinqua (n = 10 + X). At pachytene, the X chromosome is large and shows a large positively heteropyknotic telomeric region, a slim subterminal isopycnotic region and a small positively heteropyknotic telomeric region similar to Aphylla distinguenda (Figure 1G). At diakinesis and subsequent meiotic stages, the sex chromosome becomes isopycnotic with the bivalents and its size is similar to that of the median bivalents (Figure 1H). Bivalents show a terminal chiasma, and a slightly larger bivalent can be recognized, whereas the remaining ones decrease gradually and the m chromosomes are absent (Figure 1H). All prometaphases show 11 chromosomes, at metaphase II, no chromosome is observed out of the equatorial plate, and at anaphase II, all chromosomes migrate synchronously.
Phyllocycla sp. (n = 11 + X). From the early prophase II onwards, the X chromosome is large and positively heteropycnotic (Figure 1I). At pachytene the X chromosome has a large positively heteropycnotic region and a small terminal isopycnotic region (Figure 1I). Bivalents possess a single terminal chiasma and decrease gradually in size, except for the bivalent formed by the small m chromosomes, which are negatively heteropycnotic (Figure 1). At diakinesis, the X chromosome becomes isopycnotic and its size is similar to that of the median bivalents; it is hardly recognisable at prometaphase and metaphase I.
4. Discussion
Cytogenetic studies conducted on 76 species of Odonata revealed a modal number of n = 12 (11 + X) (Table 1). A reduction in modal number through fusions has been reported in five species, resulting in haploid numbers of 10 + X and 9 + X (Table 1). Interpopulation variation in chromosome number has been recorded only in two species (Asiagomphus melaenops and Trigomphus melampus), probably due to species misidentification.
Five of the 24 species of Aphylla so far described have been studied cytogenetically, showing n = 11 + X (Table 1) [1]. In A. theodorina, A. cf. distinguenda (analysed here), Ictinogomphus decoratus, I. rapax and Zonophora callipus, the median to large X chromosome is located in the centre of the mitotic metaphase plate [7,13,41,53]. This is an unusual feature as in most species with small X chromosomes, it does not adopt any particular arrangement at mitosis.
An intraindividual variation in chromosome number was detected in a specimen of Aphylla cf. distinguenda. This may be related to the fact that the testes of odonates consist of globular cysts arranged around a central duct running the length of each gonad [56,57]. A spermatogenic wave begins at a given point and then proceeds slowly towards the rest of the gonad, so that most cells in each cyst are at the same developmental stage. On this basis, the difference in the chromosome number found in the individual of Aphylla cf. distinguenda was probably due to the abnormal segregation of a bivalent at meiosis I, leading to its loss in the cell or cells that gave rise to the cysts with 10 + X analysed. Such reduction would be represented at the second meiotic division. An increase in the proportion of cells with a missing chromosome at meiosis II may be the result of a sampling error, but this is unlikely because we analysed the same number of cells at diakinesis. Another possible explanation is that individual cysts were differently affected by different environmental conditions, and that the most represented cysts were those missing one chromosome at meiosis II.
In Phyllocycla, cytogenetic studies have been performed in South American specimens from five of the 31 species so far described (Table 1) [1]. The modal number of the family is present in Phyllocycla sp. studied here and in Phyllocycla sp. studied by [5]. Souza Bueno [52] suggested a sex-determining mechanism other than X for a specimen of Phyllocycla sp. (n = 11), but it cannot be identified because the diploid number was not reported. On the other hand, Phyllocycla propinqua (n = 10 + X) shows a reduction in the number of autosomes. This was probably due to autosomal fusion in homozygous condition, as suggested by the presence of a larger bivalent not observed in other species.
Another distinct feature of the species analysed cytogenetically is the spatial arrangement of the large X chromosome at meiosis II, as it is aligned on the equatorial plate at metaphase II and migrates synchronously with the autosomes at anaphase II. In contrast, in species with small X chromosome it is usually outside the metaphase plate at metaphase II and migrates asynchronously with the autosomes (generally lying ahead) at anaphase II.
4.1. Ancestral Chromosome Number of Gomphidae
Kiauta [11] assumed that the ancestral number of the family was 2n = 25 and that the process of reduction in chromosome number occurred in three successive steps, all of which involved the sex chromosome. First, the X chromosome might have fused to an autosome (A), giving rise to the neo-XY system and reducing the chromosome number to 24. In the second step, the neo-Y (A’) chromosome probably fused to another autosome (B); this resulted in a neo-neo-Y chromosome and a neo-X/neo-neo-Y system, with the consequent reduction in the chromosome number to 23. In the third step, the autosomal portion (A) of the neo-X might have been translocated to the autosomal homologue (B’) (originating a chromosome homologous to the neo-neo-Y), thereby restoring the X0 system without change in the chromosome number (2n = 23). It is worth mentioning that the X chromosome most likely retained its original small size after these arrangements.
According to [11], the first two steps were supported by cytogenetic evidence. With regard to the third step for which no evidence was available, the author argued that it was necessary for originating the chromosome complement found in most species of Gomphidae with a detached X chromosome. Kiauta [11] cited Onychogomphus forcipatus as the primary example to support the hypothesis of chromosome number reduction from 25 to 24. The author assumed that the variation in chromosome number (12–13 elements) observed among meiotic cells of a same specimen was due to a “reversible fusion” of the X chromosome, that is to say that it was fused to an autosome in some cells and unfused in others. On the other hand, Mola [58] performed the cytological analysis of Rhionaeschna bonariensis (12 + neo-XY) and confirmed that such karyotypic variation was due to the presence of univalents derived from desynapsis of the sex bivalent. This explanation could also account for the karyotypic variation in Onychogomphus forcipatus. To support the complement reduction from 24 to 23 chromosomes, Kiauta [11] hypothesised that the X chromosome of Gomphus graslini, Ophiogomphus cecilia and Ictinogomphus rapax is large because it was formed by fusion, thereby being a neo-X. Taking into account the rearrangements proposed by this author, at meiosis are expected to observe different configurations. The first configuration is a trivalent formed by the pairing of the neo-neo-Y with the autosome B’ and the neo X. If chiasma formation fails, there are two different configurations. One of them is a heteromorphic bivalent formed by the pairing of the neo-neo-Y with the autosome B’ and a large univalent corresponding to the neo-X. The other is a heteromorphic bivalent formed by the pairing of the neo-neo-Y with the neo-X and a univalent corresponding to the autosome B’. However, Ictinogomphus rapax and Ophiogomphus cecilia show 11 homomorphic bivalents and the large X chromosome at meiosis [7,9,17,19]. Only the characteristics of the 23 mitotic chromosomes are available for Gomphus graslini [11].
Tyagi [12,47] also conducted evolutionary studies of the karyotype of Gomphidae based on species of Onychogomphus. This author included the neo-neo-X/neo-neo-Y system to the scheme proposed by Kiauta [11] and suggested that it resulted from the neo-X/neo-neo-Y through the fusion of an autosome with the neo-X, giving rise to the neo-neo-X. The existence of this neo-system was strongly suggested by the finding of a reduced chromosome number in some spermatogonial cells, and the variation in the chromosome number of different meiotic cells was assumed to derive from “unstable fusions” (i.e., “reversible fusions”).
Kiauta [11] and Tyagi [47] supported the hypothesis that the ancestral chromosome number of Gomphidae was 25 mainly due to the presence of some species with a very large X chromosome and other species with a complement of 2n = 24 and a neo-XY sex-determination system. However, the theoretical steps are not reflected in the course of meiosis and some of their observations can be interpreted from a different perspective (as mentioned above). In this context, the origins of the large X chromosome and the neo-XY sex-determination system are discussed below.
Later, Perepelov and Bugrov [17] proposed that the large X chromosome of Ophiogomphus cecilia originated from the fusion of the original X chromosome with two chromosomes of the same autosomal pair. This hypothesis seems unlikely as it would result in a genetic imbalance in both sexes: in females by the duplication of one chromosome pair and in males by the duplication of one chromosome.
Considering the discussion presented above, together with the fact that the modal chromosome number of the family is 23 (n = 11 + X) in about 86% species, we propose that the ancestral chromosome number of Gomphidae coincides with the modal chromosome number of the family.
4.2. Characterisation of the Large X Chromosome of Gomphidae
The size of the sex chromosome has been described or illustrated at the mitosis or meiosis of about 60% of Gomphidae species (Table 1). In most odonates, the X chromosome is the smallest or the second smallest of the complement if the m chromosomes are present. In Gomphidae, the X chromosome is the smallest of the complement in only two species (Gomphus vulgatissimus and Trigomphus ogumai) [14,20]. It may be the size of the smaller bivalents [20,27,28,29,34,38,53,55] or the largest of the complement [7,8,9,13,14,15,16,17,19,29,30,35,50,54], but in most cases its size is similar to that of the medium and large bivalents (Table 1). In mitosis, it may even be considerably larger (huge chromosome) than the other chromosomes of the complement (Table 1).
The distribution of the constitutive heterochromatin in the autosomes of gomphids matches with that of the other families analysed cytogenetically. The heterochromatin is found in the telomeric region of all the chromosomes (except for Nepogomphus modestus, with a bivalent lacking C-bands), and the number of repeats may vary among species, chromosomes or different telomeric regions of a same chromosome [6,17,20,22,28,36].
The X chromosome in species of other families with C-banding may be entirely C-positive, may show small C-terminal bands on one or both telomeric regions or may be isopycnotic [6]. Although the X chromosome is entirely C-positive in about half of the species analysed, this is possibly due to a higher degree of contraction (facultative heterochromatinisation in males) rather than to the presence of constitutive heterochromatin.
In Gomphidae, the amount and distribution of constitutive heterochromatin on the X chromosome have provided evidence to explain the origin of its large size. The X chromosome of Gomphus vulgatissimus is the smallest of the complement and has a low amount of heterochromatin in both telomeric regions [20]. In Shaogomphus postocularis the X chromosome presents a large terminal heterochromatic region covering about half of the chromosome and in Nihonogomphus ruptus it has large terminal heterochromatic blocks in both telomeric regions. In these two species, the size of the X chromosome is similar to that of the smaller bivalents [20]. In Paragomphus lineatus, the X chromosome is almost entirely heterochromatic and shows an euchromatic submedial region, and in Nepogomphus modestus it contains a large heterochromatic region and a small euchromatic segment in terminal position. In both species the X chromosome is of similar size to that of medium bivalents [22]. In Ophiogomphus cecilia the sex chromosome contains a large inhomogeneous heterochromatic portion and an euchromatic one with three intercalar heterochromatic segments and in Davidius fujiama it presents three large heterochromatic blocks, two of which are located in terminal position. In these two species the X chromosome is the largest of the complement. Although the other two species of Davidius were not analysed by C-banding, in meiosis their X chromosome exhibits three darker areas similar to those present in D. fujiama [15,16,17]. Intensely stained blocks can be frequently distinguished in preparations with no banding patterns, which may correspond to C bands [6].
Therefore, the heteropycnotic regions observed at prophase I in the X chromosome of Aphylla cf. distinguenda, P. propinqua and Phyllocycla sp. analysed here could be considered as regions of constitutive heterochromatin.
Despite the fact that the heterochromatin of the X chromosome has been studied in a small number of gomphid species, there is a clear trend towards an increase in heterochromatin amount with increasing X chromosome size. This allows us to propose that its large size would have originated by progressive accumulation of repetitive DNAs and heterochromatinisation rather than to fusions, as previously suggested [11,12,17,47].
4.3. Derived Sex-Determining Systems
In Odonata, no reports have been published on sex-determining systems originated by fragmentation of the X chromosome, as documented for other insects with holokinetic chromosomes such as Heteroptera and Lepidoptera [59].
In Odonata families with a small X chromosome (except Gomphidae), the identification of a heteromorphic sex bivalent at the different meiotic stages may be a difficult task, depending on both the size of the autosome with which it might have fused and on the degree of contraction of the bivalents. In about half of the species with the neo- XY system, the sex bivalent in males is homomorphic throughout meiosis and its presence can be mainly inferred from the even number of chromosomes in spermatogonial cells (Table 2). On the contrary, in the other species the sex bivalent is heteromorphic in meiosis I and II, or it is recognised only at diplotene and diakinesis (Table 2).
Neo-systems are rare, as they have been recorded in 35 species, subspecies, populations or some individuals from a population of a total of more than 600 cytogenetically analysed species of damselflies and dragonflies [4] (Table 2). They have a heterogeneous distribution and are found in only 5 species of three families of Zygoptera and in 30 species of four families of Anisoptera (Table 2). Some genera stand out by the presence of neo-systems in over 25% of their analysed species, such as Aeshna, Rhionaeschna, Onychogomphus and Orthemis [4] (Table 2).
In Gomphidae, the presence of the neo XY system is always associated with an increase in the modal diploid number of males. The increase in the diploid number may be due to an autosomal fragmentation that in homozygous condition would increase the diploid number to 25. The origin of the neo XY system is due to the fusion of the X chromosome with an autosome that would reduce the diploid number to 24. These two rearrangements may be independent, which is to say that the X chromosome does not necessarily have to fuse with one of the fragmented autosomes. The sex bivalent is the largest of the complement in the three species of Onychogomphus and in Stylurus townesi; suggesting that the fusion involved the X chromosome and the largest autosome [11,31,37,47,48]. The fact that the three species of Onychogomphus studied exhibit the same autosomal pair involved in the fusion may indicate that this rearrangement occurred in a common ancestor. In Stylurus townesi the fusion most likely had an independent origin since other three species of the genus have the modal haploid number (11 + X) of the family (Table 1). The presence of a neo-XY system in individuals of Progomphus intricatus from Brazil was postulated on the basis of the diploid number; however, its presence could not be detected at meiosis [52]. The occurrence of a chromosome number higher than the modal number of the family together with a neo-XY system has been reported not only for Gomphidae but also for Neurothemis tulia (Libellulidae); Ischnura lobata; Leptagrion macrurum (Coenagrionidae) and Heteragrion sp. b (Megapodagrionidae) [50,52,54,67,83].
In seven other species, the presence of the neo-XY system is associated with a remarkable reduction in the entire chromosome complement (diploid numbers between 6 and 16) (Table 2). However, the existence of some species (e.g., Perithemis lais (Perty, 1834), Anax guttatus (Burmeister, 1839) and Rhionaeschna intricata (Martin, 1908)) with reduced complements not involving the sex chromosome may indicate that it is not predisposed towards fusion [5,13,68].
Summarizing, the neo-XX/neo-XY sex-determining system has been found in 24 species (or 26, considering Orthemis levis and Lestes vigilax, see below), in one subspecies proposed by Kiauta [69] (Crocothemis servilia mariannae ssp. n.), in one or more populations of six species and in one or some individuals from a population of Orthemis discolor [6,53] (Table 2).
The multiple X1X1X2X2/X1X2Y system is another derived sex-determining system present in Micrathyria ungulata [18] and probably in Orthemis levis and Lestes vigilax based on the presence of a trivalent in the individuals studied [5,31]. An alternative possibility is that the latter species have a neo-XY system and an autosomal trivalent, though no heterozygosity has ever been reported for an autosomal fusion or fragmentation.
5. Conclusions
The study of the meiosis and the characteristics of the heterochromatin in the X chromosome of three species of Gomphidae, together with data from the bibliography led us to propose that the ancestral diploid number of the family was 23 and that the unusually large size of the sex chromosome was due to an increase in heterochromatin rather than to structural rearrangements, as previously claimed. We also propose that the increase in diploid number in species with neo-XY systems in gomphids originated by mechanisms of autosomal fragmentation and X-autosome fusion. Moreover, the analysis of the neo-sex determining systems allowed us to pose that two other species of odonates that present trivalents could have a multiple X1X1X2X2/X1X2Y sex-determining system.
Author Contributions
Conceptualization, L.M.M. and S.S.A.; methodology, S.S.A. and P.J.R.; Investigation, S.S.A., P.J.R., M.F.F. and L.M.M.; writing—original draft preparation, L.M.M.; writing—review and editing, S.S.A., P.J.R., M.F.F. and L.M.M.; funding acquisition, L.M.M. All authors have read and agreed to the published version of the manuscript.
Funding
This research was supported by grants from the National Council of Scientific and Technological Research (CONICET), Multi-year Investigation Project (PIP) N° 11220200102115CO.
Institutional Review Board Statement
Not applicable.
Data Availability Statement
The data presented in this study are available on request from the corresponding author.
Acknowledgments
We would like to thank to J. Muzón for the identification of the specimens of Phyllocycla propinqua and to A. Rodrigues Capítulo for the identification of the specimens of Phyllocycla sp.
Conflicts of Interest
The authors declare no conflict of interest.
References
- Novelo-Gutiérrez, R.; Ramírez, A.; González-Soriano, E. Chapter 14.2—Superfamily Gomphoidea. In Thorp and Covich’s Freshwater Invertebrates, 4th ed; Hamada, N., Thorp, J.H., Rogers, D.C., Eds.; Academic Press: Cambridge, MA, USA, 2018; Volume 3, pp. 377–397. [Google Scholar]
- Mola, L.M. Cytogenetics of American Odonata. In Odonata: Biology of Dragonflies, 1st ed.; Tyagi BK. Scientific Publishers: Jodhpur, India, 2007; pp. 153–173. [Google Scholar]
- Nokkala, S.; Laukkanen, A.; Nokkala, C. Mitotic and meiotic chromosomes in Somatochlora metallica (Corduliidae, Odonata). The absence of localized centromeres and inverted meiosis. Hereditas 2002, 136, 7–12. [Google Scholar] [CrossRef] [PubMed]
- Kuznetsova, V.G.; Golub, N.V. A checklist of chromosome numbers and a review of karyotype variation in Odonata of the world. Comp. Cytogenet. 2020, 14, 501–540. [Google Scholar] [CrossRef] [PubMed]
- Cumming, R.B. Cytogenetic Studies in the Order Odonata. Ph.D. Thesis, University of Texas, Austin, TX, USA, 1964. [Google Scholar]
- Mola, L.M.; Fourastié, M.F.; Agopian, S.S. High karyotypic variation in Orthemis Hagen, 1861 species, with insights about the neo-XY in Orthemis ambinigra Calvert, 1909 (Libellulidae, Odonata). Comp. Cytogenet. 2021, 15, 355–374. [Google Scholar] [CrossRef] [PubMed]
- Asana, J.J.; Makino, S. A comparative study of the chromosomes in the Indian dragonflies. J. Fac. Sci. Hokkaido Univ. Zool. 1935, 4, 67–86. [Google Scholar]
- Oksala, T. Zytologische Studien an Odonaten. III. Die Ovogenese. Ann. Acad. Sci. Fenn. 1945, 9, 1–132. [Google Scholar]
- Omura, T. The spermatogenesis of an Indian dragonfly, Ictinus rapax (Rambur) with special reference to the behaviour of the spermatozoa in the cyst. Biol. J. Okayama Univ. 1952, 1, 103–146. [Google Scholar]
- Kiauta, B. Morphology and kinetic behaviour of the odonate sex chromosomes, with a review of the distribution of sex determining mechanisms in the order. Genen. Phaenen. 1968, 12, 21–24. [Google Scholar]
- Kiauta, B. Sex chromosomes and sex determining mechanisms in Odonata, with a review of the cytological conditions in the family Gomphidae, and reference to the karyotypic evolution in the order. Genetica 1969, 40, 127–157. [Google Scholar] [CrossRef]
- Tyagi, B.K. Cytogenetics, karyosystematics and cytophylogeny of the Indian Odonata. Indian Rev. Life Sci. 1986, 6, 215–229. [Google Scholar]
- Ferreira, A.; Kiauta, B.; Zaha, A. Male germ cell chromosomes of thirty-two Brazilian dragonflies. Odonatologica 1979, 8, 5–22. [Google Scholar]
- Kiauta, B.; Kiauta, M. List of species, with chromosome number and preliminary notes on the karyotypes of the Odonata, collected in May, 1979 and August, 1980 by the members of the Kansai Research Group of Odonatology. Personal Communication, Utrecht, Holland, 14 July 1982. [Google Scholar]
- Suzuki, K.J.; Saitoh, K. Germ-line chromosomes of two species of Dadivíus with special reference to the sex chromosomes (Anisoptera, Gomphidae). Odonatologica 1988, 17, 275–280. [Google Scholar]
- Suzuki, K.J.; Saitoh, K. A revised chromosome study of Japanese Odonates (I). Chromosomes of 14 species belonging to nine families. Sci. Rep. Hirosaki Univ. 1990, 37, 38–49. [Google Scholar]
- Perepelov, E.; Bugrov, A.G. C-heterochromatin in chromosomes of Ophiogomphus cecilia cecilia (Four.) (Anisoptera: Gomphidae) with notes on the sex chromosome origin in the species. Caryologia 2001, 54, 169–172. [Google Scholar] [CrossRef]
- Mola, L.M.; Papeschi, A.G.; Carrillo, E.T. Cytogenetics of seven species of dragonflies. Hereditas 1999, 131, 147–153. [Google Scholar] [CrossRef]
- Perepelov, E.A.; Bugrov, A.G.; Warchałowska-Śliwa, E. C banded karyotypes of some dragonfly species from Russia. Folia Biol. 1998, 46, 137–142. [Google Scholar]
- Perepelov, E.A.; Bugrov, A.G.; Warchalowska-Sliwa, E. C-banded karyotypes of some dragonfly species from Russia. II. The families Cordulegasteridae, Corduliidae and Gomphidae. Folia Biol. 2001, 49, 175–178. [Google Scholar]
- Perepelov, E.; Bugrov, A.G. Constitutive heterochromatin in chromosomes of some Aeshnidae, with notes on the formation of the neo-XY/neo-XX mode of sex determination in Aeshna (Anisoptera). Odonatologica 2002, 31, 77–83. [Google Scholar]
- Walia, G.K.; Chahal, S.S. Distribution of constitutive heterochromatin and nucleolar organizer regions in two species of family Gomphidae (Odonata: Anisoptera). Nucleus 2014, 57, 223–227. [Google Scholar] [CrossRef]
- Kuznetsova, V.G.; Maryańska-Nadachowska, A.; Shapoval, N.A.; Anokhin, B.A.; Shapoval, A.P. Cytogenetic characterization of eight Odonata species originating from the Curonian Spit (the Baltic Sea, Russia) using C-banding and FISH with 18S rDNA and telomeric (TTAGG)n probes. Cytogenet. Genome Res. 2018, 153, 147–157. [Google Scholar] [CrossRef]
- Walia, G.K.; Devi, M. Distribution of constitutive heterochromatin in four species of genus Copera of family Platycnemididae (Odonata: Zygoptera) from India. Int. J. Life Sci. 2018, 6, 457–461. [Google Scholar]
- Garrison, R.W.; von Ellenrieder, N.; Louton, J.A. Dragonfly Genera of the New World. An illustrated and Annotated Key to the Anisoptera, 1st ed.; The Johns Hopkins University Press: Baltimore, MD, USA, 2006; 368p. [Google Scholar]
- De Gennaro, D. Análisis Meiótico y Caracterización de la Heterocromatina en Especies Argentinas de Anizoptera (Odonata). Licenciatura´s Thesis, Universidad de Buenos Aires, Buenos Aires, Argentina, 2004. [Google Scholar]
- Das, C. Studies on the association between non-homologous chromosomes during meiosis in four species of the Indian dragonflies (Odonata). J. Zool. Soc. India 1956, 8, 119–132. [Google Scholar]
- Walia, G.K.; Chahal, S.S. Linear differentiation of chromosomes of Anisogomphus bivittatus Selys, 1854 from India (Odonata: Anisoptera: Gomphidae). Int. J. Entomol. 2020, 5, 120–122. [Google Scholar]
- Kiauta, B. Cytotaxonomy of Dragonflies, with Special Reference to the Nepalese Fauna; Lectures Delivered at the Tribhuvan University, Kathmandu, II; Nepal Research Center: Kathmandu, Nepal, 1975; 78p. [Google Scholar]
- Tyagi, B.K. Studies on the Chromosomes of Odonata of Dun Valley (Dehradun, India). Ph.D. Thesis, University of Garhwal, Srinagar, 1978. In Tyagi 1982. [Google Scholar]
- Kiauta, B.; van Brink, J.M. Male chromosome complements of some Florida dragonflies, United States. Odonatologica 1978, 7, 15–25. [Google Scholar]
- Cruden, R.W. Chromosome numbers of some North American dragonflies (Odonata). Can. J. Genet. Cytol. 1968, 10, 200–214. [Google Scholar] [CrossRef] [PubMed]
- Toyoshima, H.; Hirai, H. Studies on chromosomes of four dragonflies from Kagawa Prefecture. Kagawa Biol. 1953, 1, 17–19. [Google Scholar]
- Hirai, H. Chromosomes of six species of dragonflies. Zool. Mag. 1956, 65, 198–202. [Google Scholar]
- Omura, T. A comparative study of the spermatogenesis in the Japanese dragonfly II: Family Aeschnidae, Gomphidae and Calopterygidae. Biol. J. Okayama Univ. 1957, 3, 1–86. [Google Scholar]
- Walia, G.K.; Chahal, S.S.; Singh, N. Cytogenetic studies on three species of genus Burmagomphus of family Gomphidae (Odonata: Anisoptera) from India. Intern. J. Zool. Investig. 2021, 7, 272–277. [Google Scholar]
- Tyagi, B.K. A note on the karyotypes of Burmagomphus pytamidalis Laidlow and Onychogomphus saundersi duaricus Faser (Anizoptera; Gomphidae). Odonatologica 1977, 6, 277–282. [Google Scholar]
- Kichijo, H. Chromosomes of Tachopteryx pryeri and Gomphus hakiensis (Odonata, Aeshnidae). Jpn. J. Genet. 1939, 15, 287–289. [Google Scholar] [CrossRef]
- Kiauta, B. The chromosomes of four Neotropical dragonflies from Mexico. CIS 1970, 11, 8–9. [Google Scholar]
- Kiauta, B. Notes on new or little known dragonfly karyotypes IV. Spermatocyte chromosomes of Calopterix splendens splendens (Harris) (Zygoptera. Calopterygidae), Gomphus pulchellus Selys, and Libellula depressa Linnaeus (Anisoptera: Gomphidae, Libellulidae) from Northern France. Genen. Phaenen. 1973, 16, 55–60. [Google Scholar]
- Kiauta, B.; Kiauta, M. The chromosome numbers of eleven dragonfly species from Singapore. Not Odonatol. 1982, 1, 164–165. [Google Scholar]
- Makino, S.A. comparative study of the chromosomes in the Indian dragonflies. Jpn. J. Genet. 1935, 11, 234–235. [Google Scholar] [CrossRef] [Green Version]
- Kichijo, H. Insect chromosomes. IV. Order of dragonflies, Pt. 2. Nagasaki Med. J. 1942, 10, 1639–1648, In Kuznetsova & Golub 2020. [Google Scholar]
- Dasgupta, J. Cytological studies of some Indian dragonflies. II: A study of the chromosomes during meiosis in thirty species of Indian Odonata (Insecta). Proc. Zool. Soc. 1957, 10, 1–65, In Kuznetsova & Golub 2020. [Google Scholar]
- Bagga, S. Cytology and Cytochemistry of Gametogenesis of India Dragonflies. Ph.D. Thesis, Delhi University, Delhi, India, 1961. In Tyagi 1982. [Google Scholar]
- Walia, G.K.; Sandhu, R.; Goyal, S. Cytogenetical analysis of Nepogomphus modestus from Palampur area of Himachal Pradesh, India (Gomphidae: Anisoptera). Chromosome Sci. 2006, 9, 99–100. [Google Scholar]
- Tyagi, B.K. Cytotaxonomy of the genus Onychogomphus Selys (Odonata: Anisoptera, Gomphidae), with a Special Reference to the Evolution of the Sex-Determining Mechanism and Reduced Chromosome Number in the family Gomphidae. In Proceedings of the First Indian Symposium of Odonatology; Mathavan, S., Ed.; Madurai Kamaraj University: India, 1985; pp. 217–228. [Google Scholar]
- Tyagi, B.K. The chromosome numbers and sex-determining mechanisms newly recorded in thirteen Indian dragonflies (Odonata). CIS 1978, 25, 5–7. [Google Scholar]
- Perepelov, E.; Bugrov, A.G. The constituent geterochromatin in karyotypes of dragonflies. Belyshevia 2001, 1, 10–13, In Kuznetsova & Golub 2020. [Google Scholar]
- Zhu, H.; Wu, J. Notes on the male germ cell karyotypes of some Odonata from the Shanxi Province, China. Not. Odonatol. 1986, 2, 118–120. [Google Scholar]
- Kiauta, B.; Kiauta, M.A.J.E. The chromosome numbers of some Odonata from Thailand. Not. Odonatol. 1983, 2, 27–28. [Google Scholar]
- Souza Bueno, A.M. Estudios Vromosomicos na Ordem Odonata. Master’s Thesis, Universidad Estatal Paulista, São Paulo, Brazil, 1982. [Google Scholar]
- Kiauta, B. The karyotypes of some Anisoptera from Surinam. Odonatologica 1979, 2, 267–283. [Google Scholar]
- Tyagi, B.K. Cytotaxonomy of Indian dragonflies. Indian Rev. Life Sci. 1982, 2, 149–161. [Google Scholar]
- Oguma, K. A comparative study of the spermatocyte chromosome in allied species of the dragonfly. J. Fac. Sci. Hokkaido Univ. Zool. 1930, 6, 1–32. [Google Scholar]
- Srivastava, B.K. Male reproductive organs of Crocothemis servilia servilia Drury (Libellulidae: Odonata). Zool. Anz. 1963, 170, 386–392. [Google Scholar]
- Kiauta, B. Studies on the germ cell chromosome cytology of some cytotaxonomically interesting or hitherto not studied Odonata from the autonomous region Friuli-Venezia Giulia (northern Italy). Atti. Mus. Civ. Stor. Nat. Trieste 1971, 27, 65–127. [Google Scholar]
- Mola, L.M. Post-reductional meiosis in Aeshna (Aeshnidae, Odonata). Hereditas 1995, 122, 47–55. [Google Scholar] [CrossRef]
- Mola, L.M.; Papeschi, A.G. Holokinetic chromosomes at a glance. J. Basic Appl. Genet. 2006, 17, 17–33. [Google Scholar]
- Oksala, T. Zytologische Studien an Odonaten: 1. Chromosomenverhältnisse bei der Gattung Aeschna, mit Besonderer Berücksichtigung der Postreduktionellen Teilung der Bivalente, 1st ed.; Suomalainen Tiedeakatemia: Helsinki, Finland, 1943; Volume 4, p. 64. [Google Scholar]
- Fuchsówna, J.; Sawczyńska, J. Observations on the heterochromosomes during the spermatogenesis in dragonflies (Odonata). Pt. I. Aeschna grandis L. and Libellula quadrimaculata L. Arch. Sci. Soc. 1928, 9, 177–197. [Google Scholar]
- Makalowskaja, W.N. Comparative karyological studies of dragonflies (Odonata). Arch. Russes. Anat. Histol. Embryol. 1940, 25, 24–39. [Google Scholar]
- Kiauta, B. Considerations on the evolution of the chromosome complement in Odonata. Genetica 1967, 38, 430–446. [Google Scholar] [CrossRef] [PubMed]
- Seshachar, B.R.; Bagga, S. Chromosome number and sex-determining mechanism in dragonfly Hemianax ephippiger (Burmeister). Cytologia 1962, 27, 443–449. [Google Scholar] [CrossRef] [Green Version]
- Kiauta, B. Notes on new or little known dragonfly karyotypes, 2. Male germ cell chromosomes of four East Mediterranean species: Lestes barbarus (Fabricius), Calopteryx splendens amasina Bartenev (Zygoptera: Lestidae, Calopterygidae), Caliaeschna microstigma (Schneider) and Orthetrum taeniolatum (Schneider) (Anisoptera: Aeshnidae, Libellulidae). Genen. Phaenen. 1972, 15, 95–98. [Google Scholar]
- Mola, L.M.; Papeschi, A.G. Karyotype evolution in Aeshna (Aeshnidae: Odonata). Hereditas 1994, 121, 185–189. [Google Scholar] [CrossRef]
- Ray Chaudhuri, S.P.; Dasgupta, J. Cytological studies on the Indian dragonflies I. Structure and behaviour of chromosomes in six species of dragonflies (Odonata). Proc. Zool. Soc. Bengal. 1949, 2, 81–93. [Google Scholar]
- Kiauta, B.; Kiauta, M.A.J.E. The chromosome numbers of sixteen dragonfly species from the Arun Valley, Eastern Nepal. Not. Odonatol. 1982, 9, 143–146. [Google Scholar]
- Kiauta, B. The status of the Japanese Crocothemis servilia (Drury) as revealed by karyotypic morphology (Anisoptera: Libellulidae). Odonatologica 1983, 12, 381–388. [Google Scholar]
- Yadav, J.S. A note on the karyotypic variability in Crocothemis erythraea (Brullé) and C. servilia (Drury) (Anisoptera, Libellulidae). Not. Odonatol. 1979, 1, 77–79. [Google Scholar]
- Kiauta, B.; Kiauta, M.A.J.E. On a small collection of dragonfly karyotypes from the Philippines. Odonatologica 1980, 9, 237–245. [Google Scholar]
- Kiauta, B.; Kiauta, M. Further notes on Philippine odonate karyotypes. Not. Odonatol. 1983, 2, 14–15. [Google Scholar]
- Katatani, N. On the chromosomes of dragonflies, 1. Synopsis on the studies in some Japanese dragonflies. Aeschna 1987, 20, 21–31. [Google Scholar]
- Higashi, K.; Kayano, H. The distribution of distinct karyomorphs of Crocothemis servilia Drury (Anisoptera, Libellulidae) in Kyushu and the south-western islands of Japan. Jpn. J. Entomol. 1993, 61, 1–10. [Google Scholar]
- Higashi, K.; Lee, C.E.; Kayano, H.; Kayano, A. Korea strait delimiting distribution of distinct karyomorphs of Crocothemis servilia (Drury) (Anisoptera: Libellulidae). Odonatologica 2001, 30, 265–270. [Google Scholar]
- Omura, T. A comparative study of the spermatogenesis in the Japanese dragonflies. I. Family Libellulidae. Biol. J. Okayama Univ. 1955, 2, 95–135. [Google Scholar]
- Kiauta, B.; Boyes, J.W. Cytology of ten South American Libellulidae, with cytophylogenetic consideration of the genera Orthemis Hagen and Erythrodipax Brauer (Odonata, Anisoptera). Genetica 1972, 43, 407–421. [Google Scholar] [CrossRef]
- Mola, L.M. Meiotic studies in nine species of Erythrodiplax (Libellulidae, Odonata). Neo-XY sex chromosome system in Erythrodiplax media. Cytologia 1996, 61, 349–357. [Google Scholar] [CrossRef] [Green Version]
- Agopian, S.S.; Mola, L.M. Intra and interspecific karyotype variability in five species of Libellulidae (Odonata, Anisoptera). Caryologia 1988, 41, 69–78. [Google Scholar] [CrossRef]
- Agopian, S.S.; Mola, L.M. Bandeo C en Odonata. In Proceedings of the XV Congreso de la Sociedad Argentina de Genética, Corrientes, Argentina, 16–21 September 1984; p. 17. [Google Scholar]
- Oguma, K.; Asana, J.J. Additional data to our knowledge on the dragonfly chromosome with a note on the occurrence of X-Y chromosome in the ant-lion (Neuroptera). J. Fac. Sci. Hokkaido Univ. Zool. 1932, 1, 133–142. [Google Scholar]
- Grozeva, S.M.; Marinov, M.G. Cytogenetic study of Somatochlora borisi Marinov, 2001 (Odonata: Corduliidae), and three relative species. Acta Zool. Bulg. 2007, 59, 53–58. [Google Scholar]
- Kiauta, B. The karyotype of the damselfly, Leptagrion macrurum (Burmeister, 1839), and its possible origin, with a note on the cytotaxonomic affinities of the genus (Zygoptera: Coenagrionidae). Odonatologica 1972, 1, 31–35. [Google Scholar]
Figure 1.
Aphylla cf. distinguenda (2n = 23, n = 11+ X) (A–F,K), Phyllocycla propinqua (n = 10 + X) (G,H,L) and Phyllocycla sp. (n = 11 + X) (I,J,M). A—Spermatogonial prometaphase, B—Pachytene, C—Diplotene, D—Diakinesis, E—Prophase II, F—Metaphase II with n = 11, G—Pachytene, H—Metaphase I, I—Late pachytene, J—Prometaphase I, K–M—Magnifications of X chromosomes from figures C, G, I, respectively. Arrows point isopycnotic regions. Bar: A–J = 10 um, K–M = 5 um.
Figure 1.
Aphylla cf. distinguenda (2n = 23, n = 11+ X) (A–F,K), Phyllocycla propinqua (n = 10 + X) (G,H,L) and Phyllocycla sp. (n = 11 + X) (I,J,M). A—Spermatogonial prometaphase, B—Pachytene, C—Diplotene, D—Diakinesis, E—Prophase II, F—Metaphase II with n = 11, G—Pachytene, H—Metaphase I, I—Late pachytene, J—Prometaphase I, K–M—Magnifications of X chromosomes from figures C, G, I, respectively. Arrows point isopycnotic regions. Bar: A–J = 10 um, K–M = 5 um.
Table 1.
Chromosomal data by Gomphidae species.
| Species | n (Male) | X Size in Mitosis | X Size in Meiosis | Locality | References | |
|---|---|---|---|---|---|---|
| 1 | Anisogomphus bivittatus (Selys, 1854) | 11 + X 11 + X 11 + X | - LL - | S S S | India India Nepal | [27] [28] [29] as Temnogomphus bivittatus (Selys, 1854) |
| 2 | A. occipitalis (Selys, 1854) | 11 + X | - | S - | Nepal India | [29] [30] |
| 3 | Aphylla cf. distinguenda (Campion, 1920) | 11 + X | LL | M | Argentina | [2] this work |
| 4 | A. edentata Selys, 1869 | 11 + X | - | - | Bolivia | [5] |
| 5 | A. producta Selys, 1854 | 11 + X | - | - | Bolivia | [5] |
| 6 | A. theodorina (Navas, 1933) | 11 + X | LL | LL | Brazil | [13] |
| 7 | A. williamsoni (Gloyd, 1936) | 11 + X | M | M | USA | [31] |
| 8 | Arigomphus lentulus (Needham, 1902) | 11 + X | - | - | USA | [32] as Gomphus lentulus Needham, 1902 |
| 9 | A. pallidus (Rambur, 1842) | 11 + X | - | - | USA | [5] as Gomphus pallidus Rambur, 1842 |
| 10 | A. submedianus (Williamson, 1914) | 11 + X | - | - | USA | [32] as Gomphus submedianus Williamson, 1914 |
| 11 | Asiagomphus melaenops (Selys, 1854) | 9 + X 9 + X 11 + X 11 + X | - - LL LL | - M L L | Japan Japan Japan Japan | [33] [34] [35] [14] all as Gomphus melaenops Selys, 1854 |
| 12 | Burmagomphus cf. arboreus Lieftinck, 1940 | 11 + X | - | - | India | [30] |
| 13 | B. divaricatus Lieftinck, 1964 | 11 + X | - | M | India | [36] |
| 14 | B. pyramidalis Laidlaw, 1922 | 11 + X 11 + X | - | S-M M | India India | [30,37] [36] |
| 15 | B. sivalikensis Laidlaw, 1922 | 11 + X | - | M | India | [36] |
| 16 | B. williamsoni Förster, 1914 | 11 + X | - | M | India | [36] |
| 17 | Davidius fujiama Fraser, 1936 | 11 + X 2n = 24 F | H | LL | Japan | [15] |
| 18 | D. moiwanus (Okumura, 1935) | 11+X | H | M | Japan | [15] as D. m. moiwanus (Okumura) |
| 19 | D. nanus (Selys, 1869) | 11 + X 11 + X 11 + X | - - M | S M M | Japan Japan Japan | [38] as Gomphus hakiensis Oguma, 1926 [14] [16] |
| 20 | Dromogomphus spinosus (Selys, 1854) | 11 + X | - | - | USA | [32] |
| 21 | D. spoliatus (Hagen, 1857) | 11 + X | - | - | USA | [32] |
| 22 | Epigomphus llama Calvert, 1903 | 9 + X | - | - | Bolivia | [5] |
| 23 | Erpetogomphus designatus Hagen, 1857 | 11 + X | - | - | USA | [5] |
| 24 | E. diadophis Calvert, 1905 | 11 + X | - | - | USA | [5] |
| 25 | E. ophibolus Calvert, 1905 | 11 + X | - | M | Mexico | [39] |
| 26 | Gomphoides sp. | 11 + X | - | - | Bolivia | [5] |
| 27 | Gomphus confraternus Selys, 1873 | 11 + X | - | - | USA | [32] |
| 28 | G. exilis Selys, 1854 | 11 + X 2n = 24F | - | - - | USA Canada | [32] [11] |
| 29 | G. graslini Rambur, 1842 | 11 + X | LL | - | France | [10] [11] |
| 30 | G. pulchellus Selys, 1840 | 11 + X | - | M-L | France | [40] |
| 31 | G. vulgatissimus (Linnaeus, 1758) | 11 + X | - | s | Russia | [20] |
| 32 | Ictinogomphus decoratus (Selys, 1854) | 11 + X | LL | M-L | Singapur | [41] as I. decoratus melaenops |
| 33 | I. pertinax (Hagen in Selys, 1854) | 11 + X | - | M | Japan | [14] |
| 34 | I. rapax (Rambur, 1942) | 11 + X 11 + X 11 + X | H - LL | LL - LL | India India India | [7] as Ictinus rapax [42,43,44,45] [9] as Ictinus rapax Omura 1949 |
| 35 | Nepogomphus modestus (Selys, 1878) | 11 + X 11 + X | - M | M M | India India | [46] [22] |
| 36 | Nihonogomphus ruptus (Selys, 1858) | 11 + X | - | S | Russia | [20] |
| 37 | N. viridis Oguma, 1926 | 11 + X 11 + X | - H | L L | Japan Japan | [35] [16] |
| 38 | Octogomphus specularis (Hagen, 1859) | 11 + X | - | - | USA | [32] |
| 39 | Onychogomphus forcipatus (Linnaeus, 1758) | 11 + neo-XY | Austria | [11] | ||
| 40 | O. saundersii Selys, 1854 | 11 + neo-XY | India | [12,30,37,47] as O. s. duaricus Fraser, 1924 | ||
| 41 | O schmidti Fraser, 1937 | 11 + neo-XY | India | [12,30,47,48] | ||
| 42 | Ophiogomphus bison Selys, 1873 | 11 + X/12 + X | - | - | USA | [32] |
| 43 | O. cecilia (Fourcroy, 1785) | 12 F 11 + X 11 + X | - - H | LL LL LL | Finland Russia Russia | [8] as O. serpentinus Charp. Syn Aeschna serpentina Charpentier, 1825 [19] [17] as O. c. cecilia (Four.) |
| 44 | O. colubrinus Selys, 1854 | 11 + X | - | - | USA | [32] |
| 45 | O. obscurus Bartenev, 1909 | 11 + X | - | - | Russia | [49] |
| 46 | O. occidentalis Hagen, 1882 | 11 + X | - | - | USA | [32] |
| 47 | O. rupinsulensis (Walsh, 1862) | 11 + X | - | S-M | USA | [32] |
| 48 | O spinicornis Selys, 1878 | 11 + X | - | LL | China | [50] as O. spinicorne |
| 49 | Paragomphus capricornis (Förster, 1914) | 11 + X | - | L | Thailand | [51] |
| 50 | P. lineatus (Selys, 1850) | 11 + X 11 + X 11 + X | - - L | M - M | Nepal India India | [29] [30] [22] |
| 51 | Phanogomphus lividus (Selys, 1854) | 11 + X | - | - | USA | [32] as Gomphus lividus Selys, 1854 |
| 52 | Ph. militaris (Hagen, 1858) | 11 + X | - | - | USA | [32] as Gomphus militaris Hagen, 1858 |
| 53 | Ph. spicatus (Selys, 1854) | 11 + X | - | - | USA | [32] as Gomphus spicatus Selys, 1854 |
| 54 | Phyllocycla propinqua Belle, 1972 | 10 + X | - | M | Argentina | [51] this work |
| 55 | Phyllocycla sp. | 11 + X | - | - | Bolivia | [5] |
| 56 | Phyllocycla sp. | 11 | - | - | Brazil | [52] |
| 57 | Phyllocycla sp. | 11 + X | - | M | Argentina | [2] this work |
| 58 | Phyllogomphoides undulatus (Needham, 1944) | 11 + X | - | S | Surinam | [53] |
| 59 | Progomphus borealis McLachlan, 1873 | 11 + X | - | - | USA | [32] |
| 60 | P. intricatus (Hagen, 1857) | 11 + X 11 + neo-XY | - - | - - | Bolivia Brazil | [5] [52] |
| 61 | P. obscurus (Rambur, 1842) | 11 + X | - | - | USA | [32] |
| 62 | P. phyllochromus Ris, 1918 | 11 + X | - | - | Bolivia | [5] |
| 63 | Scalmogomphus bistrigatus (Hagen, 1854) | 11 + X 11 + X | - - | LL LL | Nepal India | [29] [30,54] both as Onychogomphus bistrigatus (Hagen, 1854) |
| 64 | Shaogomphus postocularis (Selys, 1869) | 11 + X 11 + X | - - | - S | Japan Russia | [16,35] both as Gomphus postocularis Selys,1869 [20] as Gomphus epophtalmus Selys, 1872 |
| 65 | Sieboldius albardae Selys, 1886 | 11 + X 11 + X 11 + X | - H H | LL LL LL | Japan Japan Japan | [35] [14] [16] |
| 66 | Sinictinogomphus clavatus (Fabricius, 1775) | 11 + X | LL | M | Japan | [14] as Ictinogomphus clavatus (Fabricius, 1775) |
| 67 | Stylogomphus suzukii (Oguma, 1926) | 11 + X | - - | S - | Japan Japan | [55] [42] both as Gomphus suzukii Oguma, 1926 |
| 68 | Stylurus flavipes (Charpentier, 1825) | 11 + X | - | - | Russia | [48] |
| 69 | S. plagiatus (Selys, 1854) | 11 + X | - | - | USA | [32] as Gomphus plagiatus Selys, 1854 |
| 70 | S. scudderi (Selys, 1873) | 11 + X | - | - | USA | [32] as Gomphus scudderi Selys, 1873 |
| 71 | S. townesi Gloyd, 1936 | 11 + neo-XY | USA | [31] as Gomphus townesi Gloyd, 1936 | ||
| 72 | Trigomphus citimus (Needham, 1931) | 10 + X 10 + X 10 + X | - - - | - S L | Japan Japan Japan | [33] [34] [14] all as Gomphus citimus tabei Asahina, 1949 |
| 73 | T. interruptus (Selys, 1854) | 9 + X | - | L | Japan | [14] |
| 74 | T. melampus (Selys, 1869) | 9 + X 10 + X 9 + X 11 + X 10 + X | - - - - LL | M L M-L S M-S | Japan Japan Japan Japan Japan | [55] as Gomphus melampus Selys, 1869 [55] as Gomphus unifasciatus Oguma, 1926 [35] as Gomphus melampus bifasciatus Asahina [34] as Gomphus m. bifasciatus Asahina [16] |
| 75 | T. ogumai Asahina, 1949 | 10 + X | - | s | Japan | [14] |
| 76 | Zonophora callipus Selys, 1869 | 11 + X | LL | M | Surinam | [53] |
Notes: s—the smallest chromosome, S—among small chromosomes/bivalents, M—among medium chromosomes/bivalents, L—among large chromosomes/bivalents, LL—the largest chromosome/bivalent, H—huge chromosome. This table is adapted from Table 1, Gomphidae of [4], with information regarding the chromosome X length and with the addition of data of new bibliography.
Table 2.
Chromosomal data of species, subspecies, populations or individuals with derived sex determination systems.
Table 2.
Chromosomal data of species, subspecies, populations or individuals with derived sex determination systems.
| Family Suborder | 2n Male | n Male | H | SBS | N | Locality | References |
|---|---|---|---|---|---|---|---|
| Species | |||||||
| Anisoptera | |||||||
| Aeshnidae | |||||||
| Aeshna caerulea (Ström, 1783) | 11 + neo-XY | Y | SS | 2 | Finland | [60] | |
| A. grandis (Linnaeus, 1758) | 27 25 25 26 26F 26 | 13 + X 12 + X X 12 + neo-XY 12 + neo-XX 12 + neo-XY 12 + neo-XY | Y Y Y | LL LL LL | - - - 23 - 8 - | USSR USSR Finland Finland Netherlands Russia | [61] [62] [20] [8,60] [10,11,63] [21] |
| A. juncea (Linnaeus, 1758) | 26 26F 26 | 12 + X 12 + neo-XY 12 + neo-XY 12 + neo-XY | N - D Y ‡ | - - L L | - 14 3 6 4 | USSR Finland Italy Russia | [62] [60] [57] [21] |
| A.serrata Hagen, 1856 | 12 + neo-XY | N | - | 1 | Finland | [60] as A.osiliensis fennica | |
| A. viridis Eversmann, 1836 | - 26F 26 | 12 + neo-XY 12 + neo-XY | N - D ‡ | - - LL | 3 2 2 | Finland Russia | [60] [19] |
| Anax ephippiger (Burmeister, 1839) | 14 14F | 6 + neo-XY | D | M | - | India | [64] as Hemianax ephippiger |
| Caliaeschna microstigmata (Schneider, 1845) | 6 + neo-XY | N | - | 1 | Greece | [65] | |
| Gynacanta interioris Williamson, 1923 | 26 | 12 + neo-XY | D | M | 2 | Brazil | [13] |
| Rhionaeschna bonariensis (Rambur, 1842) | 26 | 12 + neo-XY | Y Y | LL LL | 5 2 | Argentina Uruguay | [58,66] both as Aeschna bonariensis |
| R. planaltica (Calvert, 1845) | 16 | 7 + neo-XY | Y | SS | 2 | Argentina | [58,66] both as Aeschna cornigera planaltica |
| Gomphidae | |||||||
| Onychogomphus forcipatus (Linnaeus, 1758) | 24 | 11 + neo-XY | Y | LL | - | Austria | [11] |
| † O. saundersii Selys, 1854 | 22? 23? | 11 + neo-XY | Y | LL | 10 | India | [37] as O. saundersi duaricus |
| O. schmidti Fraser, 1937 | 22 | 11 + neo-XY | - | LL | - | India | [47,48] |
| Progomphus intricatus (Hagen in Selys, 1858) | 23 24 | 11 + X 11 + neo-XY | - N | - - | - 3 | Bolivia Brazil | [5] [52] |
| Stylurus townesi Gloyd, 1936 | 23? | 11 + neo-XY | Y | LL | 1 | USA | [31] as Gomphus townesi |
| Libellulidae | |||||||
| Crocothemis servilia (Hagen, 1857) servilia | 25 | 12 + X | India, Nepal, China, Philippines, Japan Singapore, Korea, Thailand | [7,29,30,42,43,67,68,69,70,71,72,73,74,75] | |||
| C. servilia mariannae ssp. n. | 24 | 11 + neo-XY 11 + neo-XY 11 + neo-XY 11 + neo-XY | N D Y Y | - S SS SS | 3 5 - 25 | Japan Japan Japan Japan | [76] [69] [74] [75] |
| Elasmothemis williamsoni (Ris, 1919) | 22 | 11 + neo-XY | N | - | 2 | Surinam | [53] as Dythemis williamsoni |
| Erythrodiplax media Borror, 1942 | 22F 22 | 10 + X 11 10 + neo-XY | D | L | - 1 8 | Bolivia, Brazil Brazil Argentina | [5,13,52] [77] [78] |
| Macrothemis hemichlora (Burmeister,1839) | 6 | 2 + neo-XY | N | - | - | Bolivia | [5] |
| Micrathyria longifasciata Calvert, 1909 | 24 | 11 + neo-XY | Y | LL | 8 | Argentina | [79] |
| M. ungulata Foerster, 1907 | 23 | 10 + X1X2Y | Y | M | 2 | Argentina | [18] |
| Neurothemis tulia (Drury, 1773) | 28 | 13 + neo-XY 12 + X | Y | U | - 4 | India Thailand | [54,67] [73] all as N.t.tulia |
| Orthemis aequilibris Calvert, 1909 | 12 | 5 + neo-XY | N | - | 1 | Surinam | [53] |
| O.ambinigra Calvert, 1909 | 12 | 5 + neo-XY | N | - | 19 | Argentina | [2,6,80] |
| O. discolor (Burmeister, 1839) | 23 25 23 24 F | 11 + X 11 + neo-XY 10 + neo-XY 11 + X | 4 | Surinam Perú, Surinam, Brazil, Argentina Argentina | [53] as O. ferruginea [2,13,52,53,77] all as O. ferruginea [6] | ||
| O. levis Calvert, 1906 | 7 | 2II + III | N | - | 2 | Bolivia | [5] |
| Orthemis sp. | 10 | 4 + neo-XY | N | - | 4 | Bolivia | [5] as O. ferrugínea |
| Pseudothemis zonata (Burmeister, 1839) | - | 11 + neo-XY | Y | LL | 6 | Japan | [76] |
| Trithemis aurora (Burmeister, 1839) | 25 | 12 + X 9 + neo-XY | - | - | 4 | India Nepal | [30,81] [29] |
| Corduliidae | |||||||
| Somatochlora borisi Marinov, 2001 | 10 + neo-XY | N | - | 7 | Bulgaria | [82] | |
| Zygoptera | |||||||
| Coenagrionidae | |||||||
| Ischnura lobata Needham, 1930 | 13 + neo-XY | Y | LL | 5 | China | [50] | |
| Leptagrion macrurum (Burmeister, 1839) | 30 | neo-XY | - | - | 2 | Brazil | [83] |
| Mecistogaster sp.2 | 12 | 5 + neo-XY | N | - | - | Bolivia | [5] |
| Lestidae | |||||||
| Lestes vigilax Selys, 1862 | 9II + III | - | - | 1 | USA | [31] | |
| Megapodagrionidae | |||||||
| Heteragrion sp. b | 26 | 12 + neo-XY | D | M | 2 | Brazil | [52] |
Notes: H: heteromorphism of the sex bivalent: Y yes, N no, D until Diakinesis. ‡: With C Banding. SBS: Sex bivalent size: LL the largest of the complement, L among large bivalents, M among medium bivalents, S among small bivalents, SS the smallest of the complement, U sex chromosomes as univalents in all meiotic stages. N: number of individuals analysed. F: female. II: bivalent. III: trivalent. †: O. saundersii Selys, 1854 or Nychogomphus duaricus (Fraser, 1924). Both names were assigned by Kuznetsova and Golub [4] for the species studied by Tyagi [37] as O. saundersi duaricus.
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Mola, L.M.; Rebagliati, P.J.; Fourastié, M.F.; Agopian, S.S. Meiotic Analysis of Gomphidae Species Sheds Light on the Large X Chromosome of the Family (Anisoptera, Odonata). Diversity 2022, 14, 874. https://doi.org/10.3390/d14100874
AMA Style
Mola LM, Rebagliati PJ, Fourastié MF, Agopian SS. Meiotic Analysis of Gomphidae Species Sheds Light on the Large X Chromosome of the Family (Anisoptera, Odonata). Diversity. 2022; 14(10):874. https://doi.org/10.3390/d14100874
Chicago/Turabian StyleMola, Liliana M., Pablo J. Rebagliati, María F. Fourastié, and Silvia S. Agopian. 2022. "Meiotic Analysis of Gomphidae Species Sheds Light on the Large X Chromosome of the Family (Anisoptera, Odonata)" Diversity 14, no. 10: 874. https://doi.org/10.3390/d14100874
APA StyleMola, L. M., Rebagliati, P. J., Fourastié, M. F., & Agopian, S. S. (2022). Meiotic Analysis of Gomphidae Species Sheds Light on the Large X Chromosome of the Family (Anisoptera, Odonata). Diversity, 14(10), 874. https://doi.org/10.3390/d14100874
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