Disentangling the taxonomy of Parides burchellanus (Lepidoptera: Papilionidae) and related taxa

doi:10.21203/rs.3.rs-4208826/v1

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Disentangling the taxonomy of Parides burchellanus (Lepidoptera: Papilionidae) and related taxa

https://doi.org/10.21203/rs.3.rs-4208826/v1

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With eight described taxa, the “panthonus clade” of Parides Hübner, [1819] has been the subject of some recent taxonomic rearrangements, including the number of species that composed this clade. Based on new molecular data, including sequences of the type species of the two putative species of this group, namely Parides burchellanus (Westwood, 1872) and P. panthonus panthonus (Cramer, 1780), a new phylogenetic hypothesis is presented to this clade. The obtained phylogeny recovered the “panthonus clade” monophyletic and divided in two sub-clades. Based on this tree and genetic distances, the “panthonus clade” is composed by two species: 1) P. burchellanus, which has no recognized subspecies, and 2) P. panthonus (Cramer, 1780), with seven described subspecies. The present study provided significant contributions towards the systematics of the “panthonus clade”. As such, this marks an important first step towards supporting future studies of the ecology, biogeography, and species conservation within this clade.

Molecular systematics

Papilionidae

Parides

Taxonomy

Troidini

The neotropical butterfly Parides burchellanus (Westwood, 1872) (Papilionidae: Troidini) is an endangered species of butterfly described from an unspecified locality in Minas Gerais (Southeastern Brazil) (Mielke et al. 2004). This species was synonymized with P. panthonus jaguarae (Foetterle, 1902), a threatened butterfly, based on morphological evidence (Mielke et al. 2004). By then, the close relationship between P. burchellanus, P. panthonus (Cramer, 1780) and P. aglaope (G. Gray, [1853]) had been previously implied. D'Almeida (1966) suggested a proximity of Parides panthonus castilhoi R.F. D'Almeida, 1967 with P. aglaope based on wing pattern, and Tyler et al. (1994) recognized the affinities between P. burchellanus and P. panthonus jaguarae based on morphology and natural history. Later, in a broader molecular study, Silva-Brandão et al. (2008) confirmed that P. p. jaguarae and P. burchellanus are synonyms, suggesting that P. burchellanus is conspecific with P. panthonus. However, the absence of data on the nominal subspecies, P. panthonus panthonus (Cramer, 1780), prevented the authors from presenting a full taxonomic proposal for this clade. Recently, in the “Illustrated Lists of American Butterflies”, Warren et al. (2024) proposed that all three species, P. burchellanus (two subspecies), P. panthonus (two subspecies) and P. aglaope (five subspecies) are valid. In addition, P. burchellanus and P. panthonus jaguarae were considered as two valid subspecies of P. burchellanus, contrary to the results of Mielke et al. (2004) and Silva-Brandão et al. (2008).

With some exceptions, this clade (hereafter referred to as “panthonus clade”) includes several subspecies that are locally scarce and rare in collections. For instance, the two taxa from Southeastern Brazil are very localized, and are considered as threatened of extinction (Rosa et al. 2023). Most of the information available about the species in this clade is limited to their geographical distributions and host-plant records, with very few descriptions of immature stages (Tyler et al. 1994), and only one population study focusing on P. burchellanus (Beirão et al. 2012). Since then, a new colony of P. p. castilhoi was discovered Ilha Grande National Park (Guaíra, Paraná State, Brazil), allowing the obtaining of mitochondrial “barcode” sequences for this subspecies (Rosa et al. 2019). Finally, “barcode” sequences of two important subspecies of P. panthonus were obtained from specimens collected in French Guyana, including P. p. barbotini Brevignon, 1998 and the nominal subspecies, P. p. panthonus.

The present study aims to obtain a phylogenetic hypothesis for the “panthonus clade” to serve as the basis for a formal taxonomic proposal for this clade. This information holds significant value not only from a taxonomic standpoint but also for a better comprehension of the endangered species within this clade. Additionally, the data obtained from this study will be useful for those people and institutions involved in conservation efforts to protect butterflies and their habitats.

The taxonomy of the “panthonus clade” follows Silva-Brandão et al. (2008) where P. burchellanus and P. panthonus jaguarae are synonymous (hereafter P. burchellanus, the oldest name). Additionally, all other described taxa are considered subspecies of P. panthonus, with Parides panthonus phylarchus (Hopffer, 1865) defined as a junior synonym of Parides panthonus panthonus, based on wing pattern. Based on that, the matrix includes six out of the eight described taxa belonging to the “panthonus clade”.

Partial sequences of the 5’ extremity of the mitochondrial gene cytochrome oxidase subunit I (COI) (“barcode”) were aligned for one specimen of P. panthonus panthonus and two specimens of P. panthonus barbotini, both from French Guiana, with sequences of P. panthonus aglaope, P. panthonus castilhoi, P. burchellanus and P. panthonus lysimachus (Honrath, 1888). All sequences of Parides Hübner, [1819] available on GenBank were downloaded and aligned with sequences of P. panthonus. The final matrix had 377 taxa and 5 outgroups, namely Byasa (Atrophaneura) alcinous (Klug, 1836), Losaria (Pachliopta) neptunus (Guérin-Méneville, 1840), Troides helena (Linnaeus, 1758), Battus polydamas (Linnaeus, 1758) and Euryades corethrus (Boisduval, 1836) (Supplementary Material; Table S1). The web interface software W-IQ-TREE (Trifinopoulos et al. 2016) was used to run a maximum likelihood analysis (ML). Tree reconstruction was achieved under the best automatically discovered model scheme (GTR + F + I + G4) (Kalyaanamoorthy et al. 2017), and node supports were estimated with 1000 ultrafast bootstrap approximations (Hoang et al. 2018).

Intra- and interspecific genetic distances were also estimated for 15 species of Parides, including P. panthonus, under the model Kimura-2-parameters, in the software MEGA v. 11 (Tamura et al. 2021), in order to compare them with genetic distances within the clade panthonus.

Interspecific genetic distances within the genus Parides ranged from 0.0228 (P. ascanius (Cramer, 1775) versus P. bunichus (Hübner, [1821])) to 0.1133 (P. ascanius versus P. panares (G. Gray, [1853])) (Fig. 1). Intraspecific genetic distances varied from 0.0014 (P. ascanius, n = 142) to 0.216 (P. erithalion (Boisduval, 1836), n = 28), and was estimated as 0.0171 within the “panthonus clade”. The distances within the two clades described for the “panthonus clade” ranged from 0.0043 within “burchellanus” to 0.0133 within the clade “panthonus panthonus” (Fig. 2). Between clades (clade 1 with P. p. panthonus versus clade 2, with P. burchellanus) the distance is 0.0230.

The ML phylogenetic tree recovered the “panthonus clade” monophyletic, sister to P. lysander Cramer 1775. All sampled subspecies of the “panthonus clade” appeared organized in two clades: 1) the clade with the type subspecies, Parides p. panthonus (UFboot = 93), composed by P. panthonus panthonus, P. panthonus barbotini, P. panthonus aglaope, P. panthonus castilhoi and P. panthonus lysimachus; and 2) the clade composed by all populations of P. burchellanus (UFboot = 92), including those previously assigned to P. panthonus jaguarae (Fig. 3).

According to the available evidence, there are only two species in the “panthonus clade” of Parides, namely P. burchellanus and P. panthonus. Accordingly, all subspecies assigned to P. aglaope in Warren et al. (2024) are here transferred to P. panthonus. It is interesting to note that the wing pattern of P. burchellanus is very similar to that of P. panthonus panthonus and to some extent to P. panthonus barbotini. This similarity certainly led D'Almeida (1966) to include P. jaguarae Foetterle (1902) as a subspecies of P. panthonus (P. panthonus jaguarae) in his Catalogue of American Papilionidae.

Parides burchellanus exhibits a disjunct distribution, being found in two geographically separated regions that are more than 600 kilometers apart from each other (Beirão et al. 2012; Bedê et al. 2015), but there is no evidence of subspecies so far. However, since it is a threatened species with great potential for use as a flagship species for conservation, it would be interesting to study the genetic diversity within and between the two areas where it occurs. Such data could help to establish conservation measures for both the butterfly and its habitats, as has been done for the threatened P. ascanius (Seraphim et al. 2016).

Parides panthonus is here represented by five out of the seven described subspecies; P. panthonus ecaudatus (Joicey & Talbot, 1924) and P. panthonus callicles (H. Bates, 1861) are lacking. As previously mentioned, with a few exceptions, subspecies of P. panthonus are locally scarce and poorly represented in collections. In addition, the southernmost subspecies, P. panthonus castilhoi, is currently assessed as “Critically Endangered” (Rosa et al. 2019, 2023). Therefore, obtaining a large series of specimens to determine the actual variability of each subspecies and understand its boundaries is quite challenging (Silva-Brandão et al. 2008). It is theoretically possible to deduce the expected level of interspecific variability for these rare taxa based on data available for close congenerics, such as between the two subspecies from French Guiana (P. p. panthonus and P. p. barbotini), and between P. p. ecaudatus and P. p. lysimachus, where the only discernible distinction is in the variation in the size of the pigmented sections on their wings (see Tyler et al. 1994; Brévignon 1998 and Warren et al. 2024 for photographs of all described taxa; all studied taxa are showed in Fig. 3).

In summary, the present study has provided a well-supported taxonomic scheme for all taxa in the "panthonus clade", that served as basis for the Checklist of the “panthonus clade”, provided at the end of this section. While not all issues have been resolved, this study has provided significant contributions towards the development of a comprehensive and coherent classification system. As such, this marks an important first step towards supporting future studies of the ecology, biogeography, and conservation of species within this clade.

Check list of all taxa in the “ panthonus clade” of Parides

Parides burchellanus (Westwood, 1872) = P. panthonus jaguarae Foetterle (1902)

Parides panthonus (Cramer, 1780)

Parides panthonus panthonus (Cramer, 1780) = Parides panthonus phylarchus (Hopffer, 1865) n. syn.

Parides panthonus barbotini Brevignon, 1998

Parides panthonus aglaope (G. Gray, [1853])

Parides panthonus lysimachus (Honrath, 1888)

Parides panthonus ecaudatus (Joicey & Talbot, 1924)

Parides panthonus callicles (H. Bates, 1861)

Parides panthonus castilhoi R.F. d'Almeida, 1967

Acknowledgements

To Augusto H. B. Rosa for providing important information and pictures of the two threatened taxa in this study (Parides burchellanus and Parides panthonus castilhoi). Pictures of other subspecies of the “panthonus clade” were provided by Eduardo Carneiro (UFPR), Marcelo Duarte and Renato Silva (MZUSP) and Carlos Mielke (material from Maranhão). Eduardo P. Barbosa kindly revised the last version of the manuscript. André V.L. Freitas thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico – CNPq (fellowship 304291/2020-0), and the FAPESP (grant 2021/03868-8). This publication is part of the RedeLep «Rede Nacional de Pesquisa e Conservação de Lepidópteros» SISBIOTA-Brasil/CNPq (563332/2010-7). Christian Brévignon thanks Christophe Faynel and Thibault Rosant for providing material respectively of P. panthonus barbotini and of P. panthonus panthonus for the DNA analyses, and Rodolphe Rougerie from the Muséum national d’Histoire Naturelle de Paris for organizing these analyses. This study is registered in SISGEN (A77023D).

Author contribution Authors made substantial contributions to conception and design, and/or acquisition of data and participated in drafting the article or revising it critically for important intellectual contents.

Data availability All analyzed data is available in the supplementary material. The DNA sequences indicated in the table S1 are all available at the genbank.

Ethics approval Not applicable.

Consent to participate Not applicable.

Consent for publication Not applicable.

Competing interests The authors declare no competing interests.

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Disentangling the taxonomy of Parides burchellanus (Lepidoptera: Papilionidae) and related taxa

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