Figure - available from: PLOS ONE
This content is subject to copyright.
Source publication
It is thought that two evolutionary mechanisms gave rise to chromosomal variation in bees: the first one points to polyploidy as the main cause of chromosomal evolution, while the second, Minimum Interaction Theory (MIT), is more frequently used to explain chromosomal changes in Meliponini and suggests that centric fission is responsible for variat...
Citations
... Yet the karyotypes known of the Mycetophylax genus vary from 26 to 36 chromosomes (Cardoso et al. 2014;Micolino et al. 2022), whereas the known amplitude within the fungus-farming clade itself ranges from 8 to 54 diploid chromosomes . The asymmetry of the karyotype number and species richness across closely related groups is a conspicuous phenomenon in Hymenoptera (see Travenzoli et al. 2019) and still poorly understood. Although it is clear based on the growing evidence that chromosomal mutations may contribute to species differentiation (Rieseberg 2001), the understanding of the mechanisms and the direction and magnitude of karyotype conservation among closely related taxa is limited. ...
Trait evolution has become a central focus in evolutionary biology, with phylogenetic comparative methods offering a framework to study how and why traits vary among species. Identifying variations in trait evolution rates within phylogenies is important for uncovering the mechanisms behind these differences. Karyotype variation, which is substantial across eukaryotic organisms, plays an essential role in species diversification. This study investigates karyotype variation within the leafcutting ant clade, focusing on chromosome number and morphology. We aim to determine whether karyotypic traits are phylogenetically dependent and how different evolutionary models explain karyotype diversity. Previous models have been insufficient in explaining these variations. To address these gaps, we employ modern phylogenetic methods to assess the impact of chromosomal fissions and fusions on karyotype evolution. By evaluating various evolutionary models—particularly the Brownian motion model, which suggests neutral chromosomal changes—we pursue for the further understanding the mode and tempo of karyotype evolution in ants. Our research examines how shifts in chromosomal change rates contribute to divergence among leafcutting ant species and assesses the role of chromosomal changes in the clade's evolutionary trajectory. Comparative analysis of leafcutting ant ideograms suggests that shared karyotype traits are strongly related to species relationships. This implies that karyotype diversification in leafcutting ants follows a phylogenetic trajectory at varying rates, with differences in karyotype traits reflecting the evolutionary distance between lineages. Particularly, the increase in the chromosome number of Acromyrmex is likely due to fission rearrangements rather than demi or polyploidization. We discuss and provide insights into the mechanisms driving karyotype variation and its implications for leafcutting ant diversification.
... Additionally, it is still unclear how morphological novelties, complex social traits, and nesting preferences, among other biological features, evolved throughout the natural history of Meliponini. Additional important contributions include studies on the evolution of size-dimorphism (Quezada-Euán et al., 2019), changes in chromosome numbers (Travenzoli et al., 2019), and comparative morphology , which, although focused primarily on corbiculate bee relationships, included a representative sampling of the major stingless bee lineages. With the increasing popularization of genome-scale datasets, the application of phylogenomic methods to uncoverand increase confidence in relationships among bee lineages has become increasingly common (Romiguier et al., 2016;Bossert et al., 2017Bossert et al., , 2019Branstetter et al., 2017Branstetter et al., , 2021Freitas et al., 2021Freitas et al., , 2023Almeida, Bossert et al., 2023). ...
... Thus, chromosomal fusions may explain the karyotype variation observed in C. erecta cytotype I, as this species has a low chromosome number, whereas C. limata has high chromosome number (2n = 38), retaining repeats (TCAGG) n in the terminal regions of chromosomes. Chromosomal fusions have already been suggested to explain the chromosomal evolution of ant taxa, including fungus-growing ants of the genus Mycetophylax Emey, 1913 (Micolino et al. 2019a), leafcutting ant Acromyrmex ameliae De Souza et al. 2007, and carpenter ant Camponotus rufipes (Aguiar et al. 2017), as well as bees (Travenzoli et al. 2019b) and wasps (Menezes et al. 2014;Gokhman et al. 2019). ...
Crematogaster Lund, 1831 is a speciose ant genus globally distributed and easily recognizable. Although biogeographical theories explain some variation among Neotropical Crematogaster, several taxonomical issues remain unresolved. While cytogenetic approaches can help to delimit species, cytogenetic data are only available for 18 taxa. In this study, classical and molecular cytogenetic analyses were performed on five Crematogaster species from the Brazilian Amazon to identify species-specific patterns. Two different cytotypes, both with 2n = 22 chromosomes were observed in Crematogaster erecta Mayr, 1866, suggesting the presence of cryptic species, although with different karyotypic formulas. Crematogaster aff. erecta had 2n = 28, while Crematogaster limata Smith, 1858, Crematogaster tenuicula Forel, 1904, and Crematogaster sp. had 2n = 38. The telomeric motif (TTAGG) n was found in all five species, and the (TCAGG) n motif was detected in the telomeres of C. limata. This peculiar motif was also detected in the centromeric regions of C. erecta cytotype I. The microsatellite (GA) n was dispersed in the chromosomes of all species studied, which also had a single intrachromosomal rDNA site. The cytogenetic results revealed notable interspecific and intraspecific variation, which suggests different chromosomal rearrangements involved in the origin of these variations, also highlighting the taxonomic value of cytogenetic data on Crematogaster.
... The coverage and mapping quality of long reads to this scaffold is rather good ( Figure S1) strongly suggesting these results are not due to an assembly error. Instead, we argue this finding supports the hypothesis that multiple rearrangements involving several chromosomes occurred during the evolution of the Melipona genus resulting in its reduced haploid chromosome number [30]. It is unknown though how conserved this chromosome structure is across the genus, once size variation has been observed and heterochromatin distribution is remarkably variable across Melipona species [12,29]. ...
Background
The highly eusocial stingless bees are crucial pollinators of native and agricultural ecosystems. Nevertheless, genomic studies within this bee tribe remain scarce. We present the genome assembly of the stingless bee Melipona bicolor. This bee is a remarkable exception to the typical single-queen colony structure, since in this species, multiple queens may coexist and share reproductive duties, resulting in genetically diverse colonies with weak kinship connections. As the only known genuinely polygynous bee, M. bicolor’s genome provides a valuable resource for investigating sociality beyond kin selection.
Results
The genome was assembled employing a hybrid approach combining short and long reads, resulting in 241 contigs spanning 259 Mb (N50 of 6.2 Mb and 97.5% complete BUSCOs). Comparative analyses shed light on some evolutionary aspects of stingless bee genomics, including multiple chromosomal rearrangements in Melipona. Additionally, we explored the evolution of venom genes in M. bicolor and other stingless bees, revealing that, apart from two genes, the conserved repertoire of venom components remains under purifying selection in this clade.
Conclusion
This study advances our understanding of stingless bee genomics, contributing to the conservation efforts of these vital pollinators and offering insights into the evolutionary mechanisms driving their unique adaptations.
... The coverage and mapping quality of long reads to this scaffold is rather good ( Figure S1) strongly suggesting these results are not due to an assembly error. Instead, we argue this finding supports the hypothesis that multiple rearrangements involving several chromosomes occurred during the evolution of the Melipona genus resulting in its reduced haploid chromosome number [62]. ...
Background: The highly eusocial stingless bees are crucial pollinators of native and agricultural ecosystems. Nevertheless, genomic studies within this bee tribe remain scarce. We present the genome assembly of the stingless bee Melipona bicolor. This bee is a remarkable exception to the typical single-queen colony structure, since in this species, multiple queens may coexist and share reproductive duties, resulting in genetically diverse colonies with weak kinship connections. As the only known genuinely polygynous bee, M. bicolor genome provides a valuable resource for investigating sociality beyond kin selection.
Results: The genome was assembled employing a hybrid approach combining short and long reads, resulting in 241 contigs spanning 259 Mb (N50 of 6.2 Mb and 97.5% complete BUSCOs). Comparative analyses shed light on some evolutionary aspects of stingless bee genomics, including multiple chromosomal rearrangements in Melipona. Additionally, we explored the evolution of venom genes in M. bicolor and other stingless bees, revealing that, apart from two genes, the conserved repertoire of venom components remains under purifying selection in this clade.
Conclusion: This study advances our understanding of stingless bee genomics, contributing to the conservation efforts of these vital pollinators and offering insights into the evolutionary mechanisms driving their unique adaptations.
... In addition to identifying pathways of chromosomal evolution using phylogenetic reconstructions based on foreign characters (Cristiano et al., 2013;Micolino et al., 2019;Travenzoli et al., 2019a;Afonso Neto et al., 2022), in a number of cases, some karyotypic features can also be considered as synapomorphies that mark various clades. The phylogenetic tree of certain wasps of the family Eurytomidae, which parasitize flies that belong to Tephritidae, can be an appropriate example (Gokhman and Mikhailenko, 2008). ...
Two correlated genetic features are characteristic of the order Hymenoptera, i.e., arrhenotoky and haplodiploidy, but multiple transitions to diploid thelytoky also occurred within this group. Karyotypes of approximately two thousand members of the order are recently known. History of the chromosomal study of the Hymenoptera can be provisionally subdivided into four stages, with approximate borders of the 1930s, 1970s and 2000s between them. Although the development of this study can mainly be explained by the technical progress in preparing and analyzing chromosomal preparations, the results obtained with the help of earlier developed methods, also can successfully be used nowadays. In addition to morphometric analysis, a number of differential staining techniques are used to identify particular chromosomes and their segments; these techniques can conditionally be subdivided into two groups, the so-called “traditional” and “modern” ones. First of all, C- and AgNOR-bandings constitute the former methods; these techniques visualize heterochromatic segments and nucleolus organizing regions respectively. Moreover, modern methods are also widely used at present for studying parasitoid karyotypes. These techniques include use of fluorescent dyes (fluorochromes), especially those specifically staining AT- and GC-rich chromosome segments. Fluorescence in situ hybridization (FISH) is a very important method of physical mapping of DNA sequences on chromosomes. Immunocytochemical techniques can be of use to study chemical content and structure of chromosomes; these methods involve use of specific fluorochrome-conjugated antibodies. Nowadays, taxonomic significance of karyotypic study of the order Hymenoptera substantially increases, especially within the framework of the so-called integrative taxonomy, aimed for recognition, delimitation and description of closely related species. Furthermore, a combined use of classical and molecular methods has very good perspectives. Knowledge of hymenopteran phylogeny is necessary for identifying pathways of karyotype evolution of the order, but at least in some cases chromosome characters can be considered as synapomorphies defining different lineages. Karyotypic research also has very important implications for genetic studies of Hymenoptera. The chromosome number equals the number of linkage groups within the genome, but it also can be used as a proxy to the level of genetic recombination, especially in the context of big data approach. In addition, significance of physical mapping of DNA sequences increases in the light of the modern efforts in genome sequencing. FISH is most often used for mapping repetitive sequences, including ribosomal DNA, microsatellites and telomeric segments. Nevertheless, this technique could be useful for mapping unique sequences as well. In the order Hymenoptera, FISH is also successfully used together with chromosome microdissection for identifying particular chromosomes and/or chromosome segments, as well as various chromosomal rearrangements. In addition, chromosomal analysis can reveal the so-called supergenes, i.e., inverted chromosome segments, which accumulate genetic differences. Finally, immunocytochemical techniques can map distribution of various chemical compounds along the chromosomes, including identification of the degree of methylation of the chromosomal DNA.
... To date, it is known that chromosome numbers range from n = 8 to n = 40; however, most species have n = 17 chromosomes (Tavares et al. 2017;Cunha et al. 2021a). Through molecular and cytogenetic approaches, Travenzoli et al. (2019a) suggested that n = 17 is the ancestral chromosome number in Neotropical Meliponini, and chromosomal variations observed among the species possibly originated from Robertsonian rearrangements. Another notable cytogenetic characteristic of stingless bees is that amplifications of their heterochromatin seem to explain the increases in genome size observed among the species (Tavarez et al. 2012;Cunha et al. 2021b). ...
... (Domingues et al. 2005). As already mentioned, the chromosome number 2n = 34 is the most common and considered the probable ancestral number in Neotropical Meliponini (Travenzoli et al. 2019a). If true, it would indicate that most Trigona species maintained the ancestral chromosome number and reinforce the hypothesis that T. braueri has a derived karyotype due to chromosomal fusion. ...
... If true, it would indicate that most Trigona species maintained the ancestral chromosome number and reinforce the hypothesis that T. braueri has a derived karyotype due to chromosomal fusion. Conservation of chromosome number is a common cytogenetic trait in stingless bee genera (Tavares et al. 2017;Travenzoli et al. 2019a;Cunha et al. 2021a). Although chromosome number is highly conserved in Trigona, variations in chromosome morphology were observed in the species studied. ...
The stingless bee genus Trigona includes 32 species, exclusive to the New World, which are grouped into two clades (A and B) according to phylogenetic molecular data. Cytogenetic studies have been performed in only seven Trigona taxa, and molecular cytogenetic data are available for only one species. These studies have been important for the chromosomal characterization of the species; however, discussions focusing on the karyotype evolution of Trigona in a phylogenetic context are lacking. In this study, we characterized the karyotype, through classical and molecular cytogenetics, of five Trigona species: T. pallens and T. williana, from clade A, and T. hypogea, T. aff. fuscipennis, and T. truculenta, from clade B, in order to provide insights into the karyotype evolution in Trigona and investigate whether the analyzed cytogenetic markers may have a phylogenetic signal. All five Trigona species have 2n = 34 chromosomes. Variations in the karyotype formula were observed in T. truculenta and T. hypogea compared with the other three species. Although heterochromatin distribution was restricted to one of the arms in most of the chromosomes of the five species, C-banding experiments highlighted a lower degree of heterochromatin compaction in T. pallens and T. williana. The microsatellite (GA)15 was exclusively located in the euchromatic regions of the chromosomes in all five species. The number of pairs bearing rDNA genes varied among the species studied, and this cytogenetic trait seems to reflect the phylogeny, separating the species into two clades. This study showed interspecific variations to a greater or lesser degree among Trigona species, highlighting the intense chromosomal evolutionary dynamics in the genus.
... Based on certain heterochromatic patterns, it became the most accepted theory to explain the karyotypic variation in the whole order Hymenoptera (Hoshiba & Imai, 1993;Pompolo & Campos, 1995;Rocha et al., 2003;Godoy et al., 2013). However, recent data have pointed to an alternative direction, which from a high-numbered ancestral karyotype of n ¼ 18 for the Meliponini tribe and n ¼ 17 for the Neotropical clade, Robertsonian fusion events may have led to a decrease in chromosome number during the evolution of the stingless bees (Tavares et al., 2017;Travenzoli et al., 2019b;Cunha et al., 2021c). Corroborating this high-numbered ancestral karyotype scenario in Neotropical Meliponini, high chromosome numbers are found in phylogenetically close tribes, n ¼ 16 in Apini, n ¼ 15-21 in Euglossini, and n ¼ 12-26 in Bombini, and in other Meliponini branches, n ¼ 14-18 in Meliponini Afrotropical and n ¼ 18-20 in Meliponini Indo-Malay/Australasia (reviewed in Cunha et al., 2021b). ...
... However, some Meliponini species do not seem to fit this model, as we observed species with a high-numbered karyotype (n ¼ 17) and low heterochromatin content, such as Cephalotrigona capitata (Online Resource Figure S15). Recently, the hypothesis of chromosome fusions from a high-numbered ancestral karyotype (n ¼ 18) was suggested through meta-analyses using a molecular phylogenetic approach to explain the chromosomal evolution of the Meliponini tribe, indicating that n ¼ 17 is the putative ancestral haploid number of the Neotropical clade (Travenzoli et al., 2019b). Therefore, with the empirical cytogenetic data presented in this study, we corroborate the importance of Robertsonian fusions in the karyotype evolution of stingless bees. ...
... Based on this scenario if n ¼ 15 was the ancestral karyotype of the three Neotropical clades, fission events contributed to the increase in the chromosome number from 15 to 17 in the ancestor of clades 2 and 3. The low sampling of clade 1 species in the Travenzoli et al. (2019b) study could have underestimated the weight of n ¼ 15 as the putative ancestral karyotype. If n ¼ 17 was the ancestral karyotype of Neotropical Meliponini, evidence of the fusion events responsible for the decrease in chromosome number in the ancestor of clade 1 had already been erased by subsequent chromosomal rearrangements. ...
The Neotropical Meliponini bees, commonly known as stingless bees, are phylogenetically subdivided into three clades in which the chromosome numbers vary from n = 8 to n = 17. The goal of this study was to identify the major chromosomal rearrangements that occurred during the Neotropical Meliponini (Apidae) karyotypic evolution. In this way, we mapped 18S rDNA and five microsatellites in 33 stingless bee species collected from different Brazilian regions. The species belonged to 15 genera and showed six different chromosome numbers: n = 8, n = 9, n = 11, n = 14, n = 15, and n = 17. The 18S rDNA probe showed a variation from 2 to 12 marked chromosomes in different positions (terminal, subterminal, or centromeric), including 2 B chromosomes out of the 7 B found in Tetragonisca fiebrigi. The microsatellite (GA)15, (GAG)10, (CAA)10, and (TCAGG)6 probes formed clusters on the euchromatic regions of the chromosomes and were useful in the identification of putative Robertsonian fusion events that led to the decrease in the chromosome number during the evolution of the Neotropical Meliponini clade. (TTAGG)6 constituted the telomeric sequence of the analyzed species. The ancestral state of the three Neotropical Meliponini clades is difficult to infer, although, the putative ancestral karyotype probably had a single pair of 18S rDNA cistrons, and the decrease in chromosome number and increase in the 18S rDNA sites occurred independently between genera.
... The chromosome number observed in the five studied species (2n = 34) is concordant with that previously reported (Costa et al., 1992;Brito et al., 1997;Rocha et al., 2003;Novaes et al., 2021;Lopes et al., 2020), indicating that these species also share the most common Meliponini species chromosomal number (Tavares et al., 2017;Travenzoli et al., 2019b). Meliponini bears 2n = 34 as modal number that was considered as an apomorphy of several lineages of stingless bees, with n = 18 being the ancestral chromosome number of the tribe (Travenzoli et al., 2019b). ...
... The chromosome number observed in the five studied species (2n = 34) is concordant with that previously reported (Costa et al., 1992;Brito et al., 1997;Rocha et al., 2003;Novaes et al., 2021;Lopes et al., 2020), indicating that these species also share the most common Meliponini species chromosomal number (Tavares et al., 2017;Travenzoli et al., 2019b). Meliponini bears 2n = 34 as modal number that was considered as an apomorphy of several lineages of stingless bees, with n = 18 being the ancestral chromosome number of the tribe (Travenzoli et al., 2019b). Despite this, numerical differences related to the presence of B chromosomes were detected in some individuals of P. rustica and P. helleri, as described elsewhere (Costa et al., 1992;Tosta et al., 2004;Martins et al., 2014). ...
Repetitive DNA sequences constitute a large portion of the eukaryotic genome. Despite their importance, only a few Meliponini species, especially those from the Melipona Illiger, 1806 genus, had some microsatellite sequences and the rDNA genes physically mapped. Therefore, in order to expand our knowledge on this genomic component of neotropical bees, in the present study we investigated the distribution of microsatellite sequences, including the telomeric repeat (TTAGG)6 and rDNA clusters, in the chromosomes of five stingless species, Cephalotrigona capitata (Smith, 1854), Partamona auripennis Pedro & Camargo, 2003, P. cupira (Smith, 1863), P. helleri (Friese 1900), and Tetragona elongata (Lepeletier & Serville, 1828). The microsatellite probes (GA)15 (GAG)10, and (CAA)10, revealed hybridization signals in the euchromatic regions of most chromosome pairs. The (GAG)10 probe, however, also yielded a positive signal in the heterochromatic arm of one chromosome pair of T. elongata. The telomeric (TTAGG)6 sequence hybridized to the ends of chromosome pairs, while signals for the 18S rDNA probe varied among the species. Here was demonstrated the karyotypic diversity that exists among five species of stingless bees in terms of repetitive sequences. These cytogenetic marker provides new information about the chromatin composition and rDNA cluster locations for five Meliponini species (three genera) and highlights the contribution of repetitive sequences to the karyotypic evolution of this tribe.
... Considering that Partamona species and closely related Meliponini genera share the same diploid number (2n = 34), fission events and, consequently, increases in the number of chromosomes would not be the main model of karyotype evolution as predicted by the minimum interaction theory. Recently, alternative hypotheses have proposed a handful of rearrangements to explain karyotype evolution in the Meliponini tribe [Tavares et al., 2017;Travenzoli et al., 2019;Cunha et al., 2021b]. ...
The genus Partamona includes 33 species of stingless bees, of which 11 were studied cytogenetically. The main goal of this study was to propose a hypothesis about chromosomal evolution in Partamona by combining molecular and cytogenetic data. Cytogenetic analyses were performed on 3 Partamona species. In addition, the molecular phylogeny included mitochondrial sequences of 11 species. Although the diploid number was constant within the genus, 2n = 34, B chromosomes were reported in 7 species. Cytogenetic data showed karyotypic variations related to chromosome morphology and the amount and distribution of heterochromatin and repetitive DNA. The molecular phylogenetic reconstruction corroborated the monophyly of the genus and separated the 2 clades (A and B). This separation was also observed in the cytogenetic data, in which species within each clade shared most of the cytogenetic characteristics. Furthermore, our data suggested that the B chromosome in the genus Partamona likely originated from a common ancestor of the species that have it in clade B and, through interspecific hybridization, it appeared only in Partamona rustica from clade A. Based on the above, Partamona is an interesting genus for further investigations using molecular mapping of B chromosomes as well as for broadening phylogenetic data.