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Deadly and venomous Lonomia caterpillars are more than the two usual suspects [1]

['Camila González', 'Centro De Investigaciones En Microbiología Y Parasitología Tropical', 'Cimpat', 'Facultad De Ciencias', 'Universidad De Los Andes', 'Bogotá', 'Colombia', 'Liliana Ballesteros-Mejia', 'Institut De Systématique', 'Évolution']

Date: 2023-03

Species delimitation and taxonomic account

Our assembled database (DS-LONO2: dx.doi.org/10.5883/DS-LONO2) comprises 1,212 records of Lonomia specimens. Of these records, 69% (839 records) have DNA barcode sequences and represent all species (52) and subspecies (5) listed as valid in [25], except for “Lonomia albiguttata Köhler, 1928”, which we consider to be just an incorrect subsequent spelling of Lonomia albigutta Walker, 1855 (currently placed as a junior subjective synonym of L. obliqua). The three most recently described species, Lonomia cayennensis Brechlin & Meister, 2019, Lonomia moniqueae Brechlin & Meister, 2019, and Lonomia rubroguyana Brechlin & Meister, 2019, as well as Lonomia diabolus Draudt, 1929, recently raised to species status by [33] from subspecies status within L. achelous, are also represented by DNA barcodes. Importantly, DNA barcodes are available for the holotypes of 46 of the 60 currently valid taxon names, for the lectotypes of two further species, and for paratypes of another four species, thus providing a very robust nomenclatural foundation (see availability of type specimen DNA barcode in DS-LONO2: dx.doi.org/10.5883/DS-LONO2) for the taxonomic account proposed here.

The analysis of genetic distances and their integration with comparisons based on morphological characters (male and female genitalia, wing-patterns) revealed a rather consistent taxonomic context in which the validity of most of the currently recognized species is supported by both sets of characters. A comprehensive and detailed systematic account based on this integrative approach is currently being prepared by our group and will be the subject of a separate publication aiming at facilitating species identification within the genus. Here, we propose the preliminary recognition of three species-groups within the genus, derived mainly from comparisons of male genitalia morphology and male wing patterns and shape (see S1 Table for the list of species included in each group): the achelous-group (with modified posterior margin of the 8th abdominal sternum, strong uncus produced posteriorly, sometimes bifid, phallus lacking strong spines on the vesica); the obliqua-group (8th abdominal segment unmodified, uncus simple and laterally flattened, long valves with a distal pointed tooth, forewings with tornus rounded); and the electra-group (8th abdominal segment unmodified, long valves with an internal subdistal tooth, short uncus; large hindwings). Interestingly, although a neighbor-joining tree derived from DNA barcode data cannot be interpreted as a robust approximation of species phylogenetic relationships, they nonetheless bring congruent evidence to the division proposed above (see colored clusters in Fig 2 and S1 Table). A thorough phylogenomic analysis of phylogenetic relationships within Lonomia is in preparation and is expected to better document evolutionary relationships between and within species-groups; we thus refrain from further discussing phylogenetic relationships that may possibly be inferred from the data used here.

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TIFF original image Download: Fig 2. Circular neighbor joining tree and geographical distribution of the genus Lonomia. The inner map shows the distribution of 1019 georeferenced records of the genus Lonomia compiled in our database and gray areas represent the biomes where species with medical importance have been found. Red and orange symbols in the map, and branches in the neighbor joining tree depict the species of confirmed (red) or suspected (orange) medical importance; these are listed and numbers after the species name refer to their position on the tree. Black dots depict all the other species in the genus. Country border shape file available at: (https://gadm.org/data.html); terrestrial ecoregions of the world available at: (https://www.worldwildlife.org/publications/terrestrial-ecoregions-of-the-world). All species of the genus are numbered in the circular tree from 1 to 60 (clockwise, starting from top-left end of the tree) in reference to species as numbered in S1 Table. This tree was built using 808 DNA barcode records of more than 400bp in the public BOLD dataset DS-LONO2; branch lengths are proportional to genetic divergences (uncorrected p-distances). Colored background areas of the tree represent the three species-groups recognized in this work: the electra-group (blue), obliqua-group (yellow), and achelous-group (green). Left side picture: Lonomia sp. adult (live unidentified specimen from Costa Rica; courtesy of Armin Dett). Right side picture: Lonomia camox 6th instar caterpillar (photo by RR). A traditional vertical representation of this tree is also available at https://itol.embl.de/export/921881233420241575572285. https://doi.org/10.1371/journal.pntd.0011063.g002

Fig 2 and S1 Table provide summary statistics and graphical visualization for DNA barcode variation within and among species. In total, our integrative taxonomy study leads us to recognize 53 named and seven as yet unnamed species, distributed from Argentina to Mexico. We consider that these latter seven Operational Taxonomic Units (OTUs) represent undescribed species to which we here assign provisional names pending formal description. Two of these species are only known from caterpillars collected in Colombia (Amazonas) and Brazil (Mato Grosso) and are currently distinguished based solely on their very divergent DNA barcodes.

All 60 species can be identified by unique DNA barcodes, and we found no cases of identical DNA barcodes being shared by multiple species. We did observe two cases of species pairs sharing the same BIN (an automated registry of DNA barcode clusters in BOLD [33]) and further study is needed to assess these as potential cases of synonymy; these pairs are Lonomia pastazana Brechlin, 2017 and Lonomia siriae Brechlin & Meister, 2013; and Lonomia viksinyaevi and Lonomia pseudobliqua Lemaire, [1973]. In contrast, there are 15 species that split into multiple BINs (in grey in S1 Table), from two BINs in Lonomia belizonensis Brechlin, Meister & van Schayck, 2011 to eight BINs in Lonomia sinalectra Brechlin & van Schayck, 2015. Some of these may conceal yet unrecognized and undescribed species diversity and require further study to assess their significance.

Three subspecies were proposed by [45] and are here retained as they form distinct, though shallow, genetic clusters that are geographically segregated: Lonomia concordia conricana Brechlin & Meister, 2013 in northern Costa Rica and Lonomia concordia concordia Druce, 1886 in southern Costa Rica and Panama; Lonomia mexilectra mexpueblensis Brechlin & Meister, 2013 at relatively high elevation on the Volcanic Axis in Puebla and Oaxaca states of Mexico, and Lonomia mexilectra mexilectra Brechlin & Meister, 2011 at lower elevations along the Sierra Madre del Sur in the Mexican states of Oaxaca and Chiapas; and Lonomia quintanarooensis quinchiapasiana Brechlin & Meister, 2013, restricted to Chiapas state in Mexico, and Lonomia quintanarooensis quintanaroeensis Brechlin & Meister, 2011 distributed from southern Mexico in Quintana Roo state to Belize, Guatemala, Honduras and Guatemala (S3 Fig).

Our results also lead us to propose the following taxonomic changes:

(1) Lonomia oroiana Brechlin, Meister & Käch, 2013 syn. nov. is here synonymized with Lonomia manabiana Brechlin, Meister & Käch, 2013; under the Principle of the First Reviser as both species were described in the same publication. The DNA barcodes of holotype specimens of both species are nearly identical (p-distance of 0.6%), the male adult habitus and genitalia are morphologically very similar [46], and the species occupy the same biogeographical region, west of the Ecuadorian Andean cordillera. Additional morphological comparisons and DNA barcoding of a larger number of specimens would be necessary to address further the status of L. oroiana and so we adopt here a conservative position that limits the number of valid species within the genus.

(2) Lonomia viksinjaevi vikcuscensis Brechlin & Meister, 2013 syn. nov. is here considered to be a junior synonym of L. pseudobliqua. The type localities of vikcuscensis and pseudobliqua in Cusco and Puno departments of Peru respectively are very close (ca. 140km apart), and we found no differences between the male genitalia of the holotype of L. pseudobliqua and the illustrations of those of L. v. vikcuscensis in [45]. The wing pattern of the holotype of L. pseudobliqua is rather misleading with a yellow ground color and a double postmedial band on the forewings, which contrasts with the coloration and single postmedial band pattern observed in the holotype and two paratypes of vikcuscensis. However, similar intraspecific variation is known in other Lonomia species; for example, a Bolivian specimen of the closely related L. viksinyaevi Brechlin & Meister, 2011, preserved in the MNHN (sampleID: EL6149) has a single postmedial band, rather than the usual two of this species.

(3) Lonomia yucatensis Brechlin & Meister, 2011 syn. nov. is here synonymized with Lonomia serranoi Lemaire (2002) a species described from El Salvador that was not considered by [46] when describing L. yucatensis from the Yucatan peninsula in Mexico. DNA barcode analysis of the respective holotypes places them within a single genetic cluster (BIN: AAJ2304) distributed in southern Mexico (Oaxaca, Chiapas, Yucatan), Belize, Guatemala, Honduras and El Salvador. We found no differences in male genitalia or wing patterns between specimens from the Yucatan peninsula ([35]; specimen EL6290 at MNHN) and those from other Central American regions.

Regarding the taxonomic characterization of the only two species that have been recorded so far as being of medical importance, our results clarify the identity of L. achelous and its distinction from the recently described and closely similar species, Lonomia madrediosiana Brechlin & Meister, 2011. From the habitus and genital morphology of the male neotype of L. achelous, as well as its geographical origin in the Guiana Shield region (Suriname), we consider that specimens collected in French Guiana and in Brazilian and Colombian Amazonia (see S1 Fig), whose DNA barcodes form a cohesive genetic cluster (BOLD: ADG0261), are L. achelous. Lonomia madrediosiana was described from Madre de Dios department, Peru (see S1 Fig), and most of its records are from the eastern side of the Andes, from southern Peru (Puno department) to northern Ecuador (Sucumbíos province). However, a few specimens are also known from Ecuadorian (Orellana province) and Peruvian (Loreto department) Amazonia, which suggests that the species may extend eastward into Amazonia, where it may reach or overlap with the range of L. achelous. Lonomia madrediosiana forms a separate genetic cluster (BOLD: AAB4835) and DNA barcodes unequivocally discriminate between the two species as circumscribed here. Morphologically, we found no clear and consistent diagnostic characters in the male genitalia to distinguish the two species. However, males of L. madrediosiana have a more elongated forewing with a concave external margin. In the females, the antemedial line visible in all specimens of L. achelous is consistently absent in the L. madrediosiana that we examined (n = 6 for both species). The apex of the forewing is also more pronounced in L. madrediosiana than in L. achelous.

The second species historically recognized as being of medical importance, L. obliqua, was considered by [46] to be two distinct species that they formalized through the description of the new species, Lonomia parobliqua Brechlin, Meister & Mielke, 2011. Our results support this distinction (see Fig 2 and S1 and S2 Tables), although our integrative approach combining DNA barcodes and morphology found no support for the morphological diagnostic characters proposed by [46] and reveals an overlap of the geographical ranges of both species in southeastern Brazil (see S2 Fig). Our efforts to obtain a DNA barcode from the lectotype of L. obliqua, preserved in the Natural History Museum, London, UK (NHMUK), were in vain and we must stress that there is currently no certainty that the nomenclatural treatment of these two species is correct. Because of the medical importance of L. obliqua, we consider that it is currently best to follow the nomenclature proposed by [46] pending the further morphological and molecular studies that we consider necessary to assess species boundaries and the valid names to be used.

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[1] Url: https://journals.plos.org/plosntds/article?id=10.1371/journal.pntd.0011063

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