Open-access Revisiting the Karyotype of the Social Wasp Polistes canadensis (Linnaeus, 1758) (Hymenoptera: Vespidae: Polistinae)

Abstract

Cytogenetic techniques have been improving over the last decades, providing useful information for the systematics and evolution of several groups, such as social insects. On the other hand, karyotypic data are still incipient for most wasp genera. For instance, only 21 out of the 242 species of Polistes were karyotyped, generally with data restricted to number and morphology. Therefore, this study aimed to revisit the karyotype structure of Polistes canadensis, providing unpublished information based on traditional cytogenetic methods (karyotyping, C-banding and base-specific fluorochrome staining). Males and females of P. canadensis were characterized by haploid and diploid numbers of n=28 and 2n=56, respectively. The karyotype formula was established in 2K=18M+22SM+16A with a predominance of pericentromeric heterochromatin and terminal GC+ sites in 16 chromosome pairs. These data suggest that fissions and inversions may be involved in the group karyoevolution. It should be pointed out that our results differ significantly from the first cytogenetic report in this species, which may be related to the outdated method of obtaining mitotic chromosomes or misidentification. As a matter of fact, the improved cytogenetic methods from the present study provided reliable information about the karyotype of P. canadensis that can be used in further comparative cytotaxonomic and evolutionary analyses of social wasps.

Keywords: C-banding; Chromosomes; Cytogenetics; Heterochromatin; Polistini

HIGHLIGHTS

New chromosome number is described for the species Polistes canadensis.

Unpublished data on heterochromatic composition are recorded.

First description of C-banding for the species.

Additional information for further comparative cytotaxonomic studies in wasps are provided.

INTRODUCTION

Hymenoptera is a megadiverse order of insects with about 153,000 valid species, comprising wasps, bees and ants whose taxonomic status is usually based on morphological traits [1]. The social wasps belong to the family Vespidae, being distributed into three subfamilies: Stenogastrinae, presocial wasps (63 species), Vespinae (70 species from four genera) and Polistinae (more than 1,000 species and 25 genera) [2, 3, 4]. The species in the latter are subdivided into the tribes: Ropalidiini (290 species and four genera), Mischocyttarini (Mischocyttarus more than 250 species), Epiponini (19 genera and 250 species) and Polistini (Polistes with 242 species, 41 of them found in Brazil) [5, 6, 7]. Polistes, the only genus within Polistini, is a particularly diversified group in tropical regions but found in all biogeographic zones, except for Antarctica [8, 9, 10].

Even though several biological and ecological analyzes have been carried out in social wasps [11, 12, 13, 14], few cytogenetic reports are available for these insects, totaling about 83 karyotyped species [6, 15, among others]. In fact, the karyotypic features of many Neotropical wasps in Polistini remain unknown, particularly along Brazilian regions [16]. For instance, only 21 out of the 242 species of Polistes have been karyotyped so far [17, 5].

Even though, the few studies available indicate a high karyotypic diversity in this group of wasps, with interspecific variation from n = 9 to n = 34 chromosomes and a high rate of genomic reorganization, reinforcing the relevance of cytogenetics as a tool in species identification [18, 19, 20, 17, 15]. Thus, karyotypic analyses are useful to infer the origin and the evolution of biodiversity, particularly when incorporated with biogeographical, morphological and molecular data [21, 20, 6].

In spite of the utility of cytogenetic data in systematics [22], some peculiar features such as the high chromosomal number and small size of individuals in some species of insects, associated with technological issues, might have hindered the karyotypic characterization of this group [23]. As a result, cases of doubtful karyotypic descriptions have been reported [24, 19], reinforcing that reassessments of previous cytogenetic data based on updated methods should be carried out [23].

This seems to be the case of Polistes canadensis, since the only cytogenetic report is restricted to the determination of haploid number (n=16) based on squash technique, with no information about the chromosomal morphology or banding analyses [25]. Therefore, taking into account the scarcity of chromosomal data and the potential of karyotype studies in systematics and evolutionary inferences of insects [23] as well as the advances in cytogenetic methods, the present study aimed to provide a detailed karyotypic analysis of P. canadensis. Accordingly, we provided new data about about chromosome number and morphology, distribution of constitutive heterochromatin and location of AT/GC-rich sites in this species.

MATERIAL AND METHODS

A total of 15 nests of P. canadensis were collected from July 2019 to January 2020 (license number 35372-1 on behalf of Juvenal Cordeiro Silva Junior) at Campus II of the Universidade Estadual do Sudoeste da Bahia in the municipality of Jequié, state of Bahia (13°51'4'' S, 40°4'52' W). The adults were stored in 2 mL plastic tubes with 70% ethanol and identified by Dr. Alexandre Somavilla. The voucher specimens are stored at the Zoological Collection of Invertebrates from the Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus - AM.

Cytogenetic preparations were carried out using the cerebral ganglia of larval in the prepupae stage according to the air-drying technique Imail and coauthors [26], which consists of the fragmentation of cerebral ganglia tissue in a hypotonic solution of colchicine-sodium citrate (0.005%), followed by a series of fixatives (I, II, and III). After air-dried, the slides were stained with 10% Giemsa solution in Sörensen phosphate buffer (0.06 M; pH 6.8).

The C-banding technique was performed using the BSG method (barium hydroxide/saline solution/Giemsa) [27], with modifications [28]. For base-specific fluorochrome staining, we used Chromomycin A3 (CMA3), 4’6-diamidino-2-phenylindole (DAPI) to detect GC- and AT-rich sites, respectively, and Distamycin A as a counterstain [29].

A total of 40 slides were analyzed, representing 38 female and 2 male specimens, with an average of five metaphases each. The best metaphases were photographed using a microscope model SOLARIS-T with a portable digital camera model MEKEY. The karyotypes were arranged using Adobe Photoshop CS6. The chromosomes were organized in pairs in decreasing order of size and classified according to Levan and coauthors [30], based on centromere position.

RESULTS

The haploid and diploid numbers of P. canadensis were equal to n=28 and 2n=56 chromosomes, respectively, with a karyotype formula of 2K=18M+22SM+16A (Figure 1 A). The C-banding revealed heterochromatin segments at pericentromeric region of all chromosomes, including some centromeric signals (Figure 1 B). The base-specific fluorochrome staining technique revealed GC-rich sites (CMA3 +) at the terminal position on 15 chromosome pairs (01, 02, 03, 10, 11, 12, 13, 14, 15, 16, 17, 18, 21, 22 and 23), while AT-rich regions were not observed (Figure 1 C).

Figure 1
Karyotype of Polistes canadensis. (a) Conventional staining (female); (b) C-Banding (male); (c) Base-specific fluorochrome staining (female). GC-rich regions are shown in green. Scale = 10 µm

DISCUSSION

Previous reports revealed that variation in the chromosomal number within a single species might take place in Hymenoptera, as observed in social wasps of the tribe Epiponini and in Polistes snelleni as well as in bees of the genus Melipona and ants of the genera Myrmecia and Strumigenys [31, 24, 32, 33, 20, 34]. In some cases, distinct chromosomal numbers refer to the presence of cryptic forms or species complexes, particularly common in groups of a wide geographic range, as reported in both ants and wasps of the genus Polybia [35, 15].

Similarly, the present results (n=28) also differ significantly from the previous data available in P. canadensis since we identified 12 additional chromosome pairs in this species when compared to the pioneer study by Kerr (n=16) [25]. It should be pointed out that the former report was based on squash technique which is not as specific as air-drying method to cytogenetic analyses. Therefore, such discrepancy might represent a technical artifact. In fact, squash techniques might be harmful to chromosomes either by the rupture of sister chromatids or poor spreading of chromosomes, eventually leading to difficulties in counting chromosomes and defining their morphology [36, 37, 23]. On the other hand, air-drying techniques, as presently performed, provide reliable cytogenetic results, besides allowing a refined analysis due to the maintenance of the chromosomal structure, corroborating the reliability of the present data. Another possible explanation is the morphological misidentification of the samples analyzed by Kerr (1952) [25]. In general, insects are characterized by few diagnostic features or subtle structures for recognizing species. Some of these features might not be informative to the diagnosis of a species, hindering their identification and leading to taxonomic biases [38, 39].

Even though the karyoevolutionary trends in species of Polistes remain largely unclear by the lack of additional information, the presence of acrocentric pairs, also reported in other congeneric species [19], might derive from fissions of metacentric chromosomes, giving rise to unstable one-armed chromosomes [32]. To counteract such karyotype instability, most acrocentric chromosomes would have undergone heterochromatinization on breakage points, thus determining the appearance of pseudoacrocentric or acrocentric chromosomes [40]. Therefore, the presence of conspicuous heterochromatin blocks might mitigate putative telomere instability after centric fissions in species with derived karyotypes characterized by higher diploid numbers [26, 40, 19]. On the other hand, a thorough analyses based on a large number of species is required to evaluate whether heterochromatinization has taken place or not in Polistes, since no heterochromatin blocks were detected on short arms of acrocentric chromosomes. Alternatively, inversions could also account for the karyotypic changes observed in P. canadensis. Unfortunately, the few reports about heterochromatin distribution in related groups and most of social wasps [15, 41] hinder further inferences about the direction of chromosomal rearrangements during their karyoevolution.

Furthermore, the pattern of C-bands herein described is similar to those reported in distinct hymenopterans such as stingless bees (Meliponini), ants, social and parasitoid wasps [42, 43, 20, 15, 41]. Nonetheless, the ocurrence of heterochromatin blocks at interstitial and telomeric position as well as entirely heterochromatic arms in metacentric chromosomes have already been observed in parasitoid wasps [41]. In the case of wasps of genus Polybia, the distribution of C-bands proved to be informative for the cytogenetic differentiation of species [15, 20, 44, 45]. The few reports about C-banding in Polistes revealed two patterns: (1) predominance of centromeric heterochromatin or (2) presence of large heterochromatic segments in entire chromosomes [19]. These data along with the present results (C-bands at centromeric and pericentromeric regions) suggest that the distribution of heterochromatin in Polistes is highly variable, putatively reflecting a dynamic genomic reorganization during speciation of these wasps.

The staining with base-specific fluorochromes revealed CMA3 + signals at euchromatic regions of several chromosomal arms, indicating these regions are GC-rich (Figure 1 C), a pattern also shared by other species of the genera Mischocyttarus and Polybia [17, 46]. Nonetheless, GC+ signals have also been detected at heterochromatin regions in chromosomes of other social wasps such as Mischocyttarus consimilis and Metapolybia decorata [20, 46]. According to Menezes and coauthors [20], these regions play a key role in some groups of social wasps, once they are supposed to be involved in chromosomal rearrangements. Moreover, GC-rich sites are usually interspersed with 45S rDNA regions while the association of multiple ribosomal cistrons and centric fissions has been previously hypothesized in Hymenoptera [6]. Therefore, additional studies focusing on mapping of rDNA genes in Polistes canadensis and other species from this group are highly recommended to test this hypothesis based on a larger dataset.

CONCLUSION

In this study, we described the karyotype of Polistes canadensis including analyses of heterochromatin segments. The chromosomal number herein described differs from that available in literature and, considering the reliability of present analysis, we suggest that the present data refers to the actual karyotype of this species. We point out that this report includes the first characterization about the distribution and composition of heterochromatin and that additional studies based on a high number of species are recommended to infer the karyoevolutionary pathways in Polistes.

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  • Funding:
    This study was funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES) for financial support (code 001).

Edited by

  • Editor-in-Chief:
    Paulo Vitor Farago
  • Associate Editor:
    Marcelo Ricardo Vicari

Publication Dates

  • Publication in this collection
    31 May 2024
  • Date of issue
    2024

History

  • Received
    17 Mar 2023
  • Accepted
    18 Dec 2023
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