Research Article |
Corresponding author: Diego N. Barbosa ( barbosa.laelius@gmail.com ) Academic editor: André Nel
© 2021 Diego N. Barbosa.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Barbosa DN (2021) Phylogeny of Anisepyris Kieffer (Hymenoptera: Bethylidae: E pyrinae), with investigation of diagnostic features. Arthropod Systematics & Phylogeny 79: 189-204. https://doi.org/10.3897/asp.79.e62247
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Abstract
A cladistic analysis based on 120 morphological characters and 72 OTUs was conducted for the flat wasp genus Anisepyris Kieffer. The genus is mainly Neotropical region with few Nearctic species. The analysis retrieved well-supported relationships among the Anisepyris species and exposed the distribution of synapomorphies among the lineages, particularly concerning the mandible shape, dorsal pronotal area sulcus, and mesopleural foveae. The main diagnostic characters, described by
character evolution, cladistic analysis, morphological characters, historical distribution, Neotropical region.
Anisepyris was described by Kieffer (1906). After him,
For a genus with 254 described species (and huge potential for additional new species), “functional” subdivisions of the genus are necessary. Therefore, the “species-group” concept, even if it is not a formalized taxonomic category by the International Code of Zoological Nomenclature (ICZN), is a useful tool to for the recognition and comparison of species for alpha-taxonomic studies.
These last authors revised and described the morphological characteristics to recognize the Anisepyris species and species-groups. But no phylogenetic analysis was done to verify the monophyly, the relationships, and the evolutionary history of these “groups”. Here I propose the first phylogenetic hypothesis on the basis of morphological characters.
The goal is to describe the evolutionary history of the characters of Anisepyris and, when possible, to compare extant and fossil species, and host choice data. Furthermore, I evaluate the species-groups definitions, and discuss their relationships and the historical distribution of species.
The terms applied to the structures follow Kawada et al. (2015),
Seventy two species were selected to compose the ingroup (Table
Taxon | Species group | Collection |
---|---|---|
Outgroup | — | - |
Chlorepyris sp. 1 | — | UFES |
Laelius sp. 1 | — | UFES |
Laelius sp. 2 | — | UFES |
Ingroup | — | — |
A. aeneus Kieffer, 1906 | aeneus |
|
A. bradely (Evans, 1959) | aeneus |
|
A. tlaloc Evans, 1966 | aeneus | MCZH |
A. amrasis Barbosa & Azevedo, 2018 | aeneus | UFES |
A. barahiris Barbosa & Azevedo, 2018 | aeneus | UFES |
A. aurichalceus (Westwood, 1874) | aeneus | OXUM |
A. portoricensis Evans, 1966 | aeneus | USNM |
A. wolcotti Evans, 1959 | aeneus | USNM |
A. amazonicus (Westwood, 1874) | amazonicus | OXUM |
A. bakeri Evans, 1966 | amazonicus | USNM |
A. bregolasi Barbosa & Azevedo, 2018 | amazonicus | UFES |
A. darlingtoni Evans, 1959 | amazonicus | MCZH |
A. dominicanus Evans, 1966 | amazonicus | USNM |
A. excisus Evans, 1959 | amazonicus | MCZH |
A. jocundus Evans, 1966 | amazonicus | MCZH |
A. ramosus Santos & Azevedo, 2008 | bifidus | UFES |
A. trinitatis Evans, 1966 | bifidus | MCZH |
A. bogotensis (Kieffer, 1910) | bogotensis | ZMBH |
A. borlachi Barbosa & Azevedo, 2018 | bogotensis | UFES |
A. columbianus (Ashmead, 1893) | columbianus | UFES |
A. grandis (Ashmead, 1887) | columbianus |
|
A. nigripes Evans, 1966 | columbianus | MCZH |
A. williansi Evans, 1959 | columbianus |
|
A. arizonicus Evans, 1959 | columbianus | USNM |
A. albistigmus Evans, 1966 | columbianus | USNM |
A. alienus Evans, 1966 | columbianus | MCZH |
A. peruvianus (Kieffer, 1910) | columbianus | ZMBH |
A. insularis (Ashmead, 1894) | columbianus | USNM |
A. interruptus Santos and Azevedo, 2000 | columbianus |
|
A. penai Evans, 1966 | columbianus | MCZH |
A. similis Santos and Azevedo, 2000 | columbianus |
|
A. westwoodi (Cameron, 1888) | columbianus | BMNH |
A. analis (Cresson, 1872) | cupreolus | USNM |
A. bregoi Barbosa and Azevedo, 2018 | cupreolus | OSUC |
A. ecuadiroanus Evans, 1966 | cupreolus |
|
A. cupreolus (Evans, 1965) | cupreolus | MCZH |
A. iridescens (Evans, 1965) | cupreolus | MCZH |
A. superpilosus (Azevedo, 1993) | cupreolus | UFES |
A. indivisus Santos and Azevedo, 2000 | dietrichorum | UFES |
A. triangulatus Moreira and Azevedo, 2003 | dietrichorum | UFES |
A. annaeli Barbosa and Azevedo, 2018 | dietrichorum | UFES |
A. eoli Barbosa and Azevedo, 2018 | dietrichorum |
|
A. anduzei Evans, 1966 | franciscanus | MCZH |
A. brasilienses Evans, 1966 | franciscanus | USNM |
A. elegantulus Evans, 1966 | franciscanus |
|
A. franciscanus Evans, 1966 | franciscanus |
|
A. cepus Santos and Azevedo, 2008 | guianae | UFES |
A. guianae Evans, 1966 | guianae |
|
A. carolinianus (Evans, 1965) | megacephalus | UFES |
A. megacephalus (Ashmead, 1893) | megacephalus | USNM |
A. texanus (Evans, 1965) | megacephalus | MCZH |
A. werneri (Evans, 1965) | megacephalus | USNM |
A. amlachi Barbosa and Azevedo, 2018 | megacephalus | UFES |
A. delicatus Evans, 1966 | megacephalus | MCZH |
A. finduilasi Barbosa and Azevedo, 2018 | megacephalus |
|
A. fuinuri Barbosa and Azevedo, 2018 | megacephalus | SEAN |
A. pulchripennis (Evans, 1965) | megacephalus | USNM |
A. proteus Evans, 1966 | proteus | MCZH |
A. pollicis Santos and Azevedo, 2000 | strictus |
|
A. rectus Santos and Azevedo, 2000 | strictus |
|
A. strictus Santos and Azevedo, 2000 | strictus |
|
A. tuberosus Santos and Azevedo, 2000 | strictus |
|
A. wilsoni Evans, 1966 | strictus | MCZH |
A. eganellus (Westwood, 1874) | venustus | BMNH |
A. rotundus Santos, 2002 | venustus | UFES |
A. smithanus (Westwood, 1874) | venustus | BMNH |
A. lobatus Santos and Azevedo, 2000 | venustus | UFES |
A. venustus Evans, 1964 | venustus | MCZH |
A. attenuatus Santos, 2002 | venustus | UFES |
The analyses were based on both females and males because the species have marked sexual dimorphism. An analysis based on only one sex could not give an accurate evolutionary history for Anisepyris species. Therefore, the selection of OTUs was further narrowed down to those species known from both sexes. The choice of outgroups is justified as follows:
A total of 120 characters (Supplementary file 1) were extracted and analyzed from
The character matrix (Supplementary file 2) was produced using DELTA software (
The searches for the most parsimonious trees were carried out with the software TNT ver. 1.1 (
It has been argued that results based on properly weighted characters are preferable to those with all characters with the same weights (
The maps of distribution for each species-group were produced using the software QGIS Desktop v.3.16.0. The shapefile was based on the geographical sub-regions proposed for the Neotropical region and described by
All figures were edited in GNU Image Manipulation Program (GIMP) v.2.10.18. The phylogenetic characters were extracted from
The implied weighting analyses retrieved one most parsimonious cladogram with k = 12.153320; best score = 33.69644; steps = 928; consistency index (CI) = 0.15; and retention index (RI) = 0.47) (Fig.
The analyses under equal weight retrieved one most parsimonious cladogram. However, the phylogenetic inferences using parsimony are best achieved when carried out under differential weighting schemes (
Eleven character states were retrieved as synapomorphies for Anisepyris, eight of them were exclusive to the genus: presence of eye pilosity (#16:1) (
Three others character states were not retrieved exclusively for Anisepyris, but are important to define the genus: genitalia with T9 with very swollen apex (#55:1) (
From the Anisepyris synapomorphies in
The sub-clades in our analysis are in general agreement to the species-groups proposed by
The geographic distribution is illustrated and summarized below (Table
Anisepyris species-groups distribution A. Nearctic region; B. Me×ican Transition Zone; C. Mesoamerica; D. Antilles; E. north-western South America; F. northern Amazonia; G. south-eastern Amazonia; H. south-western Amazonia; I. Chaco; J. Paraná; K. South American Transition Zone; L. Andean region.
A | B | C | D | E | F | G | H | I | J | K | L | |
Aeneus | × | × | × | × | × | × | ||||||
Amazonicus | × | × | × | × | × | × | × | × | × | × | ||
Bifidus | × | × | × | |||||||||
Bogotensis | × | × | × | |||||||||
Columbianus | × | × | × | × | × | × | × | × | × | × | ||
Cupreolus | × | × | × | × | × | × | × | |||||
Dietrichorum | × | × | × | × | ||||||||
Franciscanus | × | × | × | × | × | × | × | |||||
Guianae | × | × | × | |||||||||
Megacephalus | × | × | × | × | × | × | × | × | × | |||
Proteus | × | × | × | × | × | × | ||||||
Strictus | × | × | × | × | × | × | × | |||||
Venustus | × | × | × | × | × | × | × | × |
Anisepyris species are unknown from the South America transitional zone or Andean region. All species-groups were recognized in the Atlantic forest (Paraná region). The amazonicus and columbianus species-groups were registered for all other regions. The megacephalus species-group had the same distribution, except for its absence from the south-western Amazonia region. The bifidus, cupreolus, dietrichorum, franciscanus, guianae, proteus, and strictus species-groups were not registered from the Antilles region. And the bifidus, bogotensis, dietrichorum, and guianae species-groups were not found in the Chaco region.
Among 11 synapomorphies of Anisepyris, only one was retrieved in correspondence with
(
According to
The genus has 35 species without metallic reflection on the body surface (
Apidae have huge species diversity in the Neotropical region, represented by 5016 species (Moure et al. 2012); many of these have iridescence, e.g., Augochlorini and Caenohalictina (Halictinae), and Euglossini (Apinae). This iridescence is generally green or blue, and in some cases, gold.
The Epyrinae are the second most diverse subfamily within Bethylidae. Within the subfamily, just like Anisepyris, the genera Bakeriella, Chlorepyris, and Laelius have species with body surface iridescent; but for Bakeriella and Laelius, most species lack metallic coloration. In Anisepyris and Chlorepyris, the majority of species have metallic coloration.
For the above mentioned Apidae, and also for Anisepyris, species diversity is related to the presence of integumental iridescence, mainly green to blue. This exemplifies the importance of the relationship between the green to blue iridescence and the forest habitat. From this scenario, the importance of the metallic coloration of the body surface for Anisepyris is clear, and is a main distinction from the other epyrine genera.
For the bethylid genera, the hairy eye is not a common character. Few inconspicuous setae are present in some species, but these do not constitute a hairy eye. The bethylid genera that have this character are the pristocerine Caloapenesia, Protisobrachium, and Pseudisobrachium (
When comparing the species distributions of Laelius Ashmead, with those of the Anisepyris species, Laelius species have a cosmopolitan distribution (
Anisepyris and Laelius were retrieved as sister-groups by
All species described from Laelius have the mandible with five distal teeth; for majority of these species, the teeth have the same width, but in some species the two most inferior teeth (in frontal view) are wider than others. For Anisepyris species the same condition is observed for all males and the majority of female specimens.
The species Anisepyris bakeri Evans, 1966 and A. bregolasi Barbosa and Azevedo, 2018, have the mandible with five distal teeth differently developed (different width among them). However, the distinction between the two superior distal teeth is observed only as an inconspicuous suture. Females specimens of the venustus and amazonicus species-groups have the mandible with four distal teeth (#6:0), all these species have the mandible with the distal teeth differently developed on their width (#7:1/2) (
The mandible distal teeth configuration, recorded here as “differently developed” (#7:1) (
The mandible distal tooth configuration, recorded here as “curved upward” (#7:2) (
For Anisepyris, the hypothesis of the “loss of superior mandible distal tooth” by the fusion between two superior distal teeth constitutes an apomorphic transformation within the genus. Hence, this could indicate that the male specimens retain the plesiomorphic characteristic, viz. “mandible with five distal teeth”. Additionally, this transformation could have arisen twice independently, in the amazonicus and venustus species-groups; and these transformations could be related with two distinct behaviors, as described above.
(
The anterior sulcus of the dorsal pronotal area is recorded in few other Bethylidae genera: Bakeriella, Holepyris, and Parascleroderma. However, the lateral sulcus of the dorsal pronotal area is recorded only for Anisepyris species.
According to Mikó et al. (2007) the muscle t1-ph1 arises from the anteromedian region of the pronotum and inserts at first phragma (at the anteromesoscutum); specifically, it arises from the anterior corner of pronotum, between the anterior (pronotal collar) and dorsal regions (dorsal pronotal area) of the pronotum. Species of Bethylidae have an articulation between the pronotum and the mesoscutum, making it possible for the pronotum to slide over the mesoscutum; this movement is aided by contraction of the muscle t1-ph1.
The presence of an external sulcus on a sclerite indicates the presence of an internal apodeme. Therefore, the apodemes represented by the anterior and lateral sulcus of the dorsal pronotal area could increase mobility between the pronotum and mesoscutum, allowing a greater range of movement in the mesosoma.
The phylogenetic signal for the characters of the mesopleural foveae was not retrieved in the topologies, because low consistence indices were retrieved for these characters, ci = 0.09–0.33. Therefore, it was more parsimonious to infer independent origins for the four characters dealing with the mesopleural foveae subdivisions (characters 35–38:1, and 99–102:1). These four characters were analyzed individually to explain their evolutionary transformations hypothesis.
Closed anterior mesopleural and mesopleural fovea
(character 35–36:1 and 99–100:1/2)
(
This character was observed in almost all species of Anisepyris and Laelius. Possibly, this character arose from the common ancestor of these two genera and is as synapomorphy for the clade (Anisepyris + Laelius).
Closed lower mesopleural fovea
(character 37:1 and 101:1)
(
According to
Unfortunately, it was not possible to accurately define this transformation, because the characteristic was retrieved arising independently among different branches of the topology. However, columbianus species-group is the only one with the “closed lower mesopleural fovea” as a synapomorphy. Thus, I hypothesize that the “closed lower mesopleural fovea” represents an apomorphic character state in relation to the “opened lower mesopleural fovea”.
Presence of Posterior mesopleural fovea
(character 38:1 and 102:1)
(
Contrary to the suggestion by
The “presence of posterior mesopleural fovea” is a common characteristic for Laelius species, the sister-group of Anisepyris. According to the definition of deep homology by
Additionally, Shubin (2009) indicated that “the deep homology of generative processes and cell-type specification mechanisms in animal development has provided the foundation for the independent evolution of a great variety of structures”. Thus, from this affirmation it was understood that the differences between “posterior mesopleural fovea” of the columbianus and venustus species-groups could be worthy of investigation for deep homology.
Unfortunately, no additional information about muscle insertions at the mesopleural foveae is available; this could give more accurate information about the evolutionary history of these foveae. The possibility to resolve the mesopleural foveae issue depends on the investigation of the transformation series among Epyrinae genera, and then to apply these to Anisepyris species evolution. This investigation could target the subdivision of mesopleural foveae, as discussed above.
(
As stated by
A large number of independent origins were retrieved within the trees. However, all these characters had substantial importance for identification and diagnosis of Anisepyris species. The use of these characters for alpha-taxonomic analyses will be useful and will contribute to taxonomy of the female specimens of Anisepyris species. The female sting characters will be more accurate after deep analyses of their features (movement, muscle, and behavior adaptation). These analyses could start firstly at higher taxonomic levels, in view to establish a hypothesis of transformations and ordination of their character states, as accomplished by
These characteristics (defined by
According to Azevedo and Azar (2012), the minimum age of Bethylidae is about 125 Ma, represented by Lancepyris opertus Azevedo and Azar (2012) from Barremian Cretaceous amber. According
As discussed by
To understand species irradiation and distribution of Anisepyris, this analysis was based on the division in sub-regions proposed by
Accessing a higher diversity of the genus from the revision by
From this, and based on the former premises above, I identify the Northern Amazonia and Paraná regions as having the highest diversity and narrowest morphological discrepancies among Anisepyris species; thus, was could propose an original distribution hypothesis to the genus. Probably, when the genus emerged in a specific area, the tendency was that diversity increased and, consequently, the character discrepancy narrowed; because, these species likely had similar niche opportunities, in view that the group persisted in these areas for a long time period. Thus, when this area does not bore adaptive niche, dispersal events were possible, the groups gained access to areas with greater opportunities, and there underwent rapid speciation, as cited by
In short, new niches imply the selection of new features and increased competition, which justifies the lower diversity; hence the more peculiar characteristics, and limited distribution of Anisepyris species in regions farther away from the hypothesized original distribution area (see
Additionally, it was observed that even the species-groups with restricted distribution, like bifidus, bogotensis, and dietrichorum, are recorded from Northern Amazonia and the Paraná region. The Paraná region, specifically, is unique in including species from all species-groups. This further supports the hypothesis that the Northern Amazonia or Paraná region could be the original distribution area for Anisepyris species; moreover, these areas are often recognized as important areas of endemism (see
This also indicates a close relationship between the Northern Amazonia and Paraná regions, in concordance with
Moreover, the discussion about the species with metallic reflection on the body surface further supports the hypothesis of the original distribution area, because these are covered by dense forests.
An interesting feature of Anisepyris distribution is the absence of species from the South American Transition Zone and Andean regions. All species registered from the Andes were related to a continuous of Amazonia forest, from the Northern Amazonia region.
The Andes mountain range had its formation about 66 million years ago, which occurred previous to the apparent origin of the Anisepyris stem group. This conformation could explain the absence of species registers in the South American Transition Zone and Andean regions, and corroborate the Northern Amazonia or Paraná regions as the original distribution area for Anisepyris species.
The historical connection between the Northern Amazonia and Paraná regions was frequently reported and described (see Pennington et al. 2010); this connection was lost in Pleistocene glacial cycles due to retraction of forest habitats and the expansion of open xerophilous vegetation.
The species-groups aeneus, amazonicus, columbianus, megacephalus, proteus, and venustus have greater diversity than the other groups. Hence, their distributions extend to the Antilles, Mesoamerica, and Nearctic regions; except the amazonicus species-group that was not registered from the Nearctic region, and the proteus species-group that was not registered from the Antilles.
From the topology retrieved (Fig.
It is interesting that these species with distribution distant from the hypothesized original distribution are have discrepant characteristics; the same was observed for species of the bogotensis species-group, related to their distribution at Antilles region. The prevalence of autapomorphies in species from outlying distributions could further support the hypothesis of the Amazonia or Paraná regions as the original distribution area for the genus.
Some Anisepyris species have their body surface without metallic reflection. The species with this characteristic were registered from the Nearctic region and Chaco region. Both regions are characterized by forests with less density, unlike the dense Amazonia and Atlantic forests. From the previous discussion about metallic reflection, insights can be gained regarding the subsequent dispersal of Anisepyris species from original distribution areas to the Chaco regions, based on the absence of metallic reflection in species registered from the Chaco region.
This scenario could be explained based on data from
Therefore, the reduced records of Anisepyris species from the Chaco region and lack of metallic reflection could be related to subsequent dispersal of these species from Amazonia and Paraná regions to Chaco region, and their consequent adaptation to niches related to lower forest density.
From the scenarios exposed above and the related geographic and morphological character distributions of Anisepyris species, the following probable ancient dispersal routes for species is proposed:
– Northern Amazonia > Paraná;
– Paraná > Northern Amazonia;
– Northern Amazonia > Chaco;
– Paraná > Chaco;
– Northern Amazonia > Antilles
– Paraná > Northern Amazonia > Antilles;
– Northern Amazonia > north-western South America > Mesoamerica > Nearctic;
– Paraná > Northern Amazonia > north-western South America > Mesoamerica > Nearctic.
Besides the hypothesis of original distribution area, and the distribution and dispersal patterns discussed above, two species-groups have discrepancies in relationship to all other groups. The bifidus species-group has its distribution recorded only from the Paraná region; and the proteus species-group, one of most diverse, has no distributions registered from the Antilles and Mesoamerica regions.
For the bifidus species-group, this could be explained based on a possible recent origin of this group. The species-group has an exclusive characteristic in comparison to the other Anisepyris species-groups; in all species the male genitalia have the paramere bifid. No other species-group shares this characteristic, which could indicate this monophyletic lineage arose recently (Fig.
For the proteus species-group, the explanation could be more complex, in view that this group has huge species diversity and wide distribution across the sub-regions of the Neotropical region. Despite the high species diversity, there is not a high diversity of morphological characteristics; contrary to that observed in other species-groups with high species diversity. Thus, it is probable that the proteus species-group’s evolutionary lineage was restricted to fewer niches, in comparison to the other species-groups. Therefore, its diversification could have favored sympatric speciation that restricted the group’s dispersal to other sub-regions, such as the Antilles and Mesoamerica regions.
Anisepyris is doubtlessly a monophyletic group, corroborating all previous works cited. Moreover, its synapomorphies were here reestablished based on a large set of species; thus, a more accurate definition for this genus was suggested.
The characteristics analyzed for the Anisepyris species-groups indicated some derived characteristics, in relation to the other Epyrinae (Bethylidae) genera. And their relationship with the distributional registers turned up some hypothesis for species distribution among the Neotropical sub-regions.
Furthermore, the transformations of the characteristics observed along the topologies could elucidate some transformation series not just for the genus, but also for the subfamily Epyrinae.
I thank Celso Oliveira Azevedo for supporting the laboratory and specimens’ access; Gabriel Augusto Rodrigues de Melo and Rodrigo Barbosa Gonçalves for providing ideas and theoretical support to the discussion; Kevin Williamns for revising and correcting English grammar; an anonymous reviewer and Evandson J. Anjos-Silva for manuscript review and comments. I also acknowledge grants from Fundação de Amparo à Pesquisa do Espírito Santo (FAPES), #3935842/2007 and #41106407/2008, for the scholarships granted to the author.
File 1
Data type: .doc
Explanation note: Characters of females – Characters not applicable to taxa for which only male specimens are available.
File 2
Data type: .xlsx
Explanation note: Data matrix of morphological characters.