Corresponding author: Alexandre Somavilla ( alexandre.s@hotmail.com ) Corresponding author: Rodolpho S. T. Menezes ( rstmenezes@gmail.com ) Academic editor: Mónica M. Solórzano Kraemer
© 2021 Alexandre Somavilla, Paulo C. S. Barroso, Marcos Aragão, Sidnei Mateus, Rodolpho S. T. Menezes.
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:
Somavilla A, Barroso PCS, Aragão M, Mateus S, Menezes RST (2021) An integrative taxonomic and phylogenetic approach reveals a new Neotropical swarm-founding social wasp, Pseudopolybia cryptica sp. n. (Vespidae: Polistinae: Epiponini). Arthropod Systematics & Phylogeny 79: 25-35. https://doi.org/10.3897/asp.79.e64304
|
Phenotypic characters are traditionally the main information for species discrimination in taxonomic studies of invertebrates. However, the presence of inter- and intraspecific polymorphism makes it difficult to identify species in many groups such as Neotropical social wasps. Herein, we examined different sources of biological information such as adult morphology, male genitalia, nest architecture, and genetic data applying an integrative taxonomic approach to study pinned museum specimens belonging to the social wasp genus Pseudopolybia de Saussure, 1863. Based on multiple independent lines of evidence, we described a new Neotropical swarm-founding social wasp, Pseudopolybia cryptica sp. n. Moreover, we proposed a phylogenetic hypothesis for Pseudopolybia including this new species. Our taxonomic findings applying an integrative approach reinforce that the social wasp diversity in the Neotropics may be underestimated due to morphological similarity.
Epiponini, integrative taxonomy, molecular systematics, mtDNA, paper wasps, Pseudopolybia, social wasps, species delimitation
Accurate species delimitation is essential for multiple disciplines such as ecology, evolution, conservation biology, among others (
Pseudopolybia de Saussure, 1863 is a Neotropical genus of swarm-founding social wasps (Vespidae: Polistinae: Epiponini) comprising four species: Pseudopolybia compressa (de Saussure, 1854), Pseudopolybia difficilis (Ducke, 1905), Pseudopolybia langi Bequaert, 1944, and Pseudopolybia vespiceps (de Saussure, 1863). They are distinguished by the third segment of the labial palpi bearing a short, stout, curved bristle near its apex, and the number of palpal segments being six maxillary and four labial (
Although there are only four described species within Pseudopolybia several taxonomic problems persist (e.g.
In the present paper, we use an integrative taxonomic approach, i.e. analyzing the variation of mitochondrial genetic markers with molecular species delimitation methods, adult morphology, nest architecture, and male genitalia, to assess the taxonomic status of pinned museum specimens previously identified as P. compressa from Central-West and Northeast of Brazil. Based on multiple independent lines of evidence, we described a new Neotropical swarm-founding social wasp, Pseudopolybia cryptica sp. n.
Three colonies from the new species were collected during a survey in Central-West and Northeast of Brazil in the years 1997, 2000, and 2008 by SM in the Brazilian states of Mato Grosso and Bahia. We analyzed a total of 83 Pseudopolybia specimens deposited in the Invertebrate Collection of Instituto Nacional de Pesquisas da Amazônia (
For adult morphological structures and male genitalia we used the terminology following the original descriptions,
Additionally, we produced a distribution map for Pseudopolybia species based on a compilation of literature and collection records from museums (see Supplementary material
We followed standard laboratory protocols (
Phylogenetic inference was conducted by maximum likelihood using IQ-TREE (ver. 1.6.12, see http://www.cibiv.at/software/iqtree;
We carried out single-locus molecular species delimitation analyses with three methods based on different approaches: a sequence similarity clustering method, the automatic barcode gap discovery (ABGD) (
Based on our integrative taxonomic approach, we can hypothesize that Pseudopolybia specimens collected in the Brazilian states of Mato Grosso and Bahia belong to a new species that we describe below. We consider several morphological characters including male genitalia (Fig.
Morphological differences between P. compressa (de Saussure, 1854) and Pseudopolybia cryptica sp. n.
Morphological characters | P. compressa (de Saussure) | P. cryptica sp. n. |
General color | black, extensive yellow marks | black, few yellow marks mainly on the face |
Frontal furrow | narrow | deep |
Distance between the lateral ocelli | short, less than the diameter of the ocelli | larger, equal to the diameter of the ocelli |
Pronotal carina, in the middle region | lower | high |
Tegula shape | elongated | globose |
Posterior margin of the propodeum and orifice of the propodeal muscle | elevated | not elevated |
Propodeal valve | translucid | not translucid |
Tergum I–VI | black, with or without yellow apical band, sparse bristles | entire dark brownish, row of bristles |
Aedeagus, apical portion | fine denticulation | intermediate denticulation |
Aedeagus, lateral apodema | with a projection in the central curvature | without a projection in the central curvature |
Paramere, spine base | with long and dense bristles | with long and sparse bristles |
Digitus | with dense bristles | with sparse bristles |
Nova Mutum, Mato Grosso, Brazil.
Female (Fig.
Pseudopolybia cryptica Somavilla & Menezes, new species. A: Female, lateral view. B: Female, dorsal view. C: Female face, frontal view. D: Male face, frontal view. E-I: Male genitalia. E: Paramere inner view. F: Aedeagus ventral view. G: Aedeagus lateral view. H: Digitus lateral view. I: Cuspis lateral view.
Male (Fig.
(Fig.
Color black, with few yellow marks mainly on the face and mandibles, clypeus, inner orbits, base of antennal scape, antennal pedicel and gena; clypeus wider than long, in contact with the eyes by less than the width of the antennal socket; frontal furrow deep; tegula globose; tergum I–VI dark brownish; sternum dark brownish; tergum and sternum without apical yellow bands.
The specific epithet “cryptica” refers to the Greek word kryptikos that means hidden because the species was previously classified as Pseudopolybia compressa.
Approximate range of the new species is shown in Fig.
Type material
: Holotype ♀, ‘Brasil, Mato Grosso | Nova Mutum, Buriti Farm | 13°51′90.3″S, 056°11′61.9″W | 23.viii.2000, Nest, S. Mateus leg.’ (
The new species is reconstructed as sister to P. compressa based on the analysis of partial sequences of COI and 16S and morphological characters (Fig.
Phylogeny of Pseudopolybia inferred from the combined Maximum likelihood analysis of molecules (mitochondrial markers COI and 16S) and morphology, with molecular species delimitation analyses ABGD, bPTP, and mPTP (vertical bars). Values below to the nodes represent ultrafast bootstrap (left) and SH-aLRT (right) supports as reported by IQ-Tree.
The following key is a revised and adapted version with few modifications of the key provided by
1 | Dorsal pronotal carina is very weak; first metasomal segment much longer than wide; eyes densely haired; small species (approximately 6–8 mm); yellow with three brown stripes on the scutum; metasoma brownish |
P. langi
Bequaert (Fig. |
1’ | Dorsal pronotal carina lamellate laterally; first metasomal tergum nearly as broad as or much broader than long; eyes with or without hairs; larger species (approximately 13–15 mm); yellow to black | 2 |
2 | The first and second metasomal segment a little longer than wide; metanotum not compressed; yellow with black marks on the head and mesosoma; three black stripes on the scutum; metasoma brownish |
P. difficilis
(Ducke) (Fig. |
2’ | The first and second metasomal segment approximately twice as wide as long; metanotum slightly to strongly compressed; dark yellow with three black stripes on the scutum or blackish species with pale marks | 3 |
3 | Dark yellow species with brown to blackish marks; prestigma much longer than wide; clypeus narrowly separated from eyes; eyes bare; the tip of the clypeus weakly pointed; metanotum slightly compressed; the malar space longer than fourth antennal article |
P. vespiceps
(de Saussure) (Fig. |
3’ | Blackish species with pale marks; prestigma approximately as long as wide; clypeus touching the eyes; eyes with hairs; the tip of the clypeus sharply pointed; metanotum strongly compressed; the malar space about as long as fourth antennal article | 4 |
4 | Blackish species with wide pale marks in the face; pronotal carina lower in the middle region; tegula elongated with an inferior yellow spot; tergum I–VI black, with or without a yellow apical band, sparse bristles |
P. compressa
(de Saussure) (Fig. |
4’ | Blackish species with few pale marks in face; pronotal carina high in the middle region; tegula more globose entirely black; tergum I-VI entire dark brownish, row of bristles |
P. cryptica sp. n (Fig. |
The phylogenetic inference using a concatenated matrix (morphology and mitochondrial DNA) is summarized in Fig.
The evolutionary divergences of COI and 16S using K2P are given in Supplementary Table S3. The average genetic distance within Pseudopolybia for COI was 12.09% and 16S was 7.8%. Pseudopolybia cryptica differs from P. compressa by a genetic distance of more than 8% for COI and 3.3% for 16S. The intraspecific genetic distance for COI and 16S within P. compressa range from 0.0%–3.36% and 0.47%, respectively (Supplementary Table S3). The ABGD, bPTP, and mPTP methods consistently identify P. cryptica as a distinct hypothetical species and also the other Pseudopolybia species already described (see bars in Fig.
Our integrated evaluation of adult morphology, male genitalia, nest architecture, and results from molecular species delimitation support the new species P. cryptica and indicate a sister species relationship with P. compressa. From the morphological point of view, P. cryptica cannot be confused with any Pseudopolybia species, except for P. compressa (Fig.
Concerning our molecular data, the species delimitation analyses have been carried out with a clustering (ABGD) and tree-based (bPTP and mPTP) methods on two mitochondrial markers, COI and 16S. Empirical studies have shown that species delimitation methods based on single-locus data tend to under- and oversplit species (
Despite several studies performed molecular species delimitation approaches to identify Hymenoptera species (
A.S. and R.S.T.M. designed the study, funding acquisition, project administration, and led the writing of the manuscript. P.C.S.B. carried out the molecular laboratory work under supervision of R.S.T.M. S.M. collected samples. A.S., R.S.T.M., P.C.S.B., and M.A. performed the analyses. All authors gave final approval for publication.
We are thankful to Dr. Gavin Broad and Dr. Jaswinder Boparai for support in Natural History Museum (London). We also are grateful to Mr. José Mario Ribeiro Mendes, the owner of Buriti Farm in Nova Mutum, Mato Grosso, for sampling permit in its farm and hospitality. AS is thankful to the Fundação de Amparo à Pesquisa do Estado do Amazonas (FAPEAM – FIXAM, process number 062.01427/2018) and REFAUNA-MCTIC Program for financial support. RSTM is grateful to the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) process number #2015/02432-0 and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) by grant no. 431249/2018-0. PCSB is thankful to CNPq for a scholarship (132264/2018-8). MA is thankful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior for a scholarship (88887.492572/2020-00).