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Research Article
A new species of Nephus (Nephus) (Coleoptera, Coccinellidae) described from Reunion Island
expand article infoAlexandra Magro‡§, Julissa Churata-Salcedo|, Emilie Lecompte‡, Jean-Louis Hemptinne‡§, Lucia M. Almeida|
‡ Laboratoire Evolution et Diversité Biologique, Toulouse, France
§ ENSFEA, Castanet-Tolosan, France
| Universidade Federal do Paraná, Curitiba, Brazil
¶ Université Toulouse III-Paul Sabatier, Toulouse, France

Corresponding author: Lucia M. Almeida ( lalmeida51@gmail.com )

Academic editor: Janakiraman Poorani
© 2020 Alexandra Magro, Julissa Churata-Salcedo, Emilie Lecompte, Jean-Louis Hemptinne, Lucia M. Almeida.
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: Magro A, Churata-Salcedo J, Lecompte E, Hemptinne J-L, Almeida LM (2020) A new species of Nephus (Nephus) (Coleoptera, Coccinellidae) described from Reunion Island. ZooKeys 962: 123-137. https://doi.org/10.3897/zookeys.962.51520
ZooBank: urn:lsid:zoobank.org:pub:3A37A055-1B1E-4B5B-A6B5-518BDE44A334
Open Access

Abstract

We report here a new species belonging to Nephus (Nephus) Mulsant. Nephus (Nephus) apolonia sp. nov. was collected in the Reunion Island (Mascarene Archipelago, Indian Ocean). We describe this new species and redescribe and illustrate three other Nephus species already known from Reunion: Nephus (Nephus) oblongosignatus Mulsant, 1850, Nephus (Geminosipho) reunioni (Fürsch, 1974) and Nephus (Nephus) voeltzkowi Weise, 1910. Furthermore, we present a phylogenetic tree for these four species and calculate the genetic distances between them, using high-throughput DNA sequencing of the mitochondrial genome. The similar external morphology of N. apolonia sp. nov. and N. voeltzkowi very probably explains why individuals from the first species have been mistakenly identified as the latter and were not recognized as different until now. Other than external and genitalia traits, the present study provides molecular evidence confirming these are indeed two different species.

Keywords

Coccinelloidea, ladybird beetle, molecular data, predator, Scymnus, systematics

Introduction

The Coccinellidae is a diversified family composed of some 6000 species, and the largest of the superfamily Coccinelloidea (Robertson et al. 2015). Seago et al. (2011) formally recognised two subfamilies within the Coccinellidae, Microweisinae and Coccinellinae sensu Ślipiński (2007). This last subfamily includes most of the Coccinellidae tribes, among them the Coccidulini sensu Seago et al. (2011), to which Nephus belongs. Nephus was first considered by Mulsant (1846) as a subgenus of Scymnus but Mader (1924) and then eventually Pope (1957) treated it as a valid genus.

The following characters distinguish Nephus: antennae with nine or pseudo-11 antenomeres; prosternal process sub-quadrangular, as wide as long, with a shallow lateral depression, without carina; legs with tarsi trimerous; abdomen with six ventrites, with incomplete postcoxal line, recurved and not reaching posterior margin of first ventrite.

According to Gordon (1976, 1985), Nephus has five subgenera: Depressoscymnus Gordon, Nephus Mulsant, Scymnobius Casey, Sidis Mulsant, and Turboscymnus Gordon; some of them have been considered as valid genera (Gordon and González 2002, Giorgi and González 2014). Fürsch (1987) described the subgenus Geminosipho and indicated the following species, Nephus (Geminosipho) bielawskii Fürsch, N. (Geminosipho) fenestratus (Sahlberg), N. (Geminosipho) koltzei (Weise). The same author (1987, 2007) considered eight Nephus subgenera: Bipunctatus Fürsch, 1987, Depressoscymnus Gordon, 1976, Geminosipho Fürsch, 1987, Nephus Mulsant, 1846, Parascymnus Chapin, 1965, Scymnobius Casey, 1899, Sidis Mulsant, 1850 and Turboscymnus Gordon, 1976.

Fürsch (2007), in his Catalogue of the African species of Nephus, reports 80 species belonging to four Nephus subgenera: Nephus, Sidis, Geminosipho, and Bipunctatus. Concerning specifically Reunion Island, Chazeau et al. (1974) mentioned three species, at that time considering Nephus as a subgenus of Scymnus: Scymnus (Nephus) voeltzkowi Weise, 1910, Scymnus (Nephus) oblongosignatus Mulsant, 1850 and Scymnus (Nephus) reunioni Fürsch, 1974. Poussereau et al. (2018) also mention these three species.

In this contribution, we describe a fourth Nephus (Nephus) species for Reunion Island, and redescribe the three already known species based on the study of a number of specimens of each species and using molecular data.

Material and methods

The specimens examined here were provided by the first author from a laboratory rearing (Laboratoire Evolution & Diversité Biologique, Université Toulouse III) initiated from field collected material: Nephus oblongosignatus and N. voeltzkowi were collected in Reunion Island in 2011, N. apolonia sp. nov. was collected in Reunion Island in 2013, and N. reunioni was collected in 2007 in Portugal, where the species had been introduced for biological control in the 1980’s (Magro et al. 1999). The first author also observed specimens collected from 2006 to 2012 by the Insectarium of Reunion to investigate possible misidentifications of N. apolonia sp. nov. with N. voeltzkowi and to gather additional information on the geographical distribution of the new species on Reunion Island.

Photographs of the external morphology as well as male and female genitalia were taken using a Leica DMC 2900 Digital Camera attached to Leica M205C stereomicroscope using Leica Application Suite. Furthermore, specimens were examined with a JEOL JSM-6360LV scanning electron microscope in the Electronic Microscopy Center of Universidade Federal do Paraná. The length and width measurements of the species represent the average of the examined specimens.

The terminology used in the descriptions follows Ślipiński (2007). Labels of the type specimens are arranged in sequence from top to bottom, where the data for each label are within double quotes (“”), a slash (/) separates the rows, and information between brackets ([]) provides additional details written on the labels.

Examined material is deposited in the following collections: Coleção Entomológica Pe. J.S. Moure, Universidade Federal do Paraná, Curitiba, Paraná, Brazil (DZUP) and in Muséum National d’Histoire Naturelle, Paris, France (MNHN).

We used the mitochondrial genome of Nephus species previously sequenced by Magro et al. (2020): N. reunioni, N. includens, N. voeltzkowi and N. apolonia sp. nov. (voucher number: NeSpa1), together with the mitogenome of N. oblongosignatus sequenced in the present study (accession numbers: see Table 1) following the same protocol (see details in Magro et al. 2020).

Molecular characterization and distance analyses were conducted on the cytochrome c oxidase I (COI) gene using MEGA v.7 (Kumar et al. 2016). Pairwise distances were estimated between specimens using the Kimura-2-parameters model (Kimura 1980). We reconstructed the phylogenetic relationships between the Nephus species based on the mitogenome sequences (all protein coding and tRNA genes, but we deleted the control region because of the high divergence between species and the presence of repeated sequences, leading to low quality alignments in this region), using as outgroup the available sequence of Cryptolaemus montrouzieri which belongs to the same tribe as Nephus (i.e., Coccidulini sensu Seago et al. 2011) together with other Coccinellidae species (accession numbers: see Table 1). Sequences were aligned using MAFFT default parameters (Katoh and Standley 2013). We inferred maximum likelihood trees and bootstrapping with RAxML 8.2.10 (Stamatakis 2014) under the best-fitting model of sequence evolution for the dataset (GTR+G model), selected using the Akaike information criterion (AIC) using jModelTest 2 (Darriba et al. 2012).

Table 1.
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Genbank accession numbers for the mitogenome sequences used in the analysis.

Species Genbank accession
Nephus apolonia sp. nov. MN164644
Nephus reunioni MN164643
Nephus includens MN164642
Nephus voeltzkowi MN164645
Nephus oblongosignatus MT445723
Propylea japonica KM244660
Harmonia axyridis KR108208
Cryptolaemus montrouzieri KT874575
Henosepilachna pusillanima KJ131489

Results and discussion

The species of Nephus present the following characteristics: antennae with nine or pseudo-11 antenomeres (Fig. 1A–D); prosternal process sub-quadrangular, as wide as long, with a shallow lateral depression, without carina (Fig. 1E–H); legs with tarsi trimerous (Fig. I–L); abdomen with six ventrites in males and females, with incomplete postcoxal line, recurved and not reaching posterior margin of the first ventrite (Fig. 1M–P).

Key to species of Nephus from Reunion Island

1 Each elytron black with one spot 2
1’ Each elytron black with two spots (Fig. 3) Nephus (Geminosipho) reunioni (Fürsch, 1974)
2 Body rounded, oblong; each elytron with one yellowish oblong spot (Fig. 2) Nephus (Nephus) oblongosignatus Mulsant, 1850
2’ Body elongated, each elytron with one yellowish elongated spot 3
3 Each elytron black with one big oval yellowish elongated spot, reaching middle of elytron; spermatheca with sharp base and truncated apex (Fig. 4) Nephus (Nephus) voeltzkowi Weise, 1910
3’ Each elytron black with one small irregular yellowish spot, not reaching middle of elytron; spermatheca with sharp base and truncated apex (Fig. 5) Nephus (Nephus) apolonia Magro & Almeida, sp. nov.

Descriptions of species

Nephus (Nephus) oblongosignatus Mulsant, 1850

Figs 1, 2

Scymnus oblongosignatus Mulsant, 1850: 960 (original description).

Nephus oblongosignatus: Sicard 1909: 145–146; Weise 1910: 513.

Nephus grinerae Sicard, 1909: 145 (original description); Korschefsky 1931: 152 (synonymy).

Scymnus (Nephus) oblongosignatus: Korschefsky 1931: 152; Chazeau et al. 1974: 273 (systematics).

Nephus (Nephus) oblongosignatus: Poussereau et al. 2018: 130 (systematics).

Diagnosis

Nephus oblongosignatus is similar to N. voeltzkowi and N. apolonia sp. nov. but differs in the body shape, size and shape of the spots and the pattern of genitalia.

Description

Male. Length 1.77 mm, width 1.28 mm. Body oval, oblong, with short fine whitish pubescence. Integument of pronotum, scutellar shield and elytra black (Fig. 2A). Elytra with one yellowish oblong spot on each elytron. Pronotum black, antero-lateral border dark brown (Fig. 2A, D). Head dark brown, antennae and mouthparts yellowish (Fig. 2B, D). Meso- and metaventrite light brown. Epipleuron light brown, without excavations to receive femora. Legs with coxae and femora dark brown, tibiae and tarsi light brown (Fig. 2B, C). Abdomen light brown; postcoxal line incomplete (Figs 1M, 2E) and last ventrite emarginated (Fig. 2F).

Figure 1. 

Scanning electron microscopy A–D antennae E–H prosternal process I–L tarsi M–P abdominal postcoxal line A, E, I, M Nephus (Nephus) oblongosignatus Mulsant, 1850 B, F, J, N Nephus (Geminosipho) reunioni (Fürsch, 1974) C, G, K, O Nephus (Nephus) voeltzkowi Weise, 1910 D, H, L, P Nephus apolonia Magro & Almeida, sp. nov.

Genitalia with tegmen, penis guide, phallobase and parameres symmetrical. Spicule long (Fig. 2G). Penis guide shorter than parameres, sharp at apex (Fig. 2H, J). Parameres articulated with phallobase, distant from each other, strongly widened at apex, with long bristles along parameres (Fig. 2H, I). Penis sclerotized, J-shaped, with sharp apex, penis capsule T-shaped and elongated (Fig. 2J, K).

Figure 2. 

Nephus (Nephus) oblongosignatus Mulsant, 1850 A dorsal view B ventral view C lateral view D frontal view E, F abdomen G–K male genitalia: G spicula H, I tegmen (dorsal and lateral view) J, K penis L, M female genitalia: L spermatheca M coxites.

Female. Length 1.79 mm, width 1.34 mm. Similar to male. Genitalia with coxites longer than wide, subtriangular, 3.0× longer than wide; stylus mamiliform with long bristles (Fig. 2M). Spermatheca with thick walls, slightly arched, not very striated, and marked by one strong constriction in the middle; with sharp base and truncated apex (Fig. 2L).

Material examined

Reunion Island: First generation from a laboratory rearing (Laboratoire Evolution & Diversité Biologique, Université Toulouse III) initiated from field material collected in November 2011 in Manapany-les-Bains, 19 specimens [DZUP].

Nephus (Geminosipho) reunioni (Fürsch, 1974)

Figs 1, 3

Scymnus (Nephus) reunioni Fürsch, 1974: 275 (original description).

Nephus (Sidis) reunioni Fürsch 2007: 5 (systematics).

Nephus (Geminosipho) reunioni: Poussereau et al. 2018: 132 (systematics).

Diagnosis

Nephus reunioni differs from the other species in the number, shape and size of the spots and the pattern of genitalia.

Description

Male. Length 1.7 mm, width 1.28 mm. Body oval, with short fine whitish pubescence. Integument of pronotum, scutellar shield and elytra black (Fig. 3A). Elytra with two yellowish transverse spots on each elytron, arranged in a row; elytra apex yellowish (Fig. 3A). Pronotum black, anterior border dark brown (Fig. 3A, D). Head dark brown, antennae and mouthparts yellowish (Fig. 3B). Meso- and metaventrite dark brown. Epipleuron black, without excavations to receive femora. Legs with coxae dark brown and femora, tibiae and tarsi yellowish (Fig. 1J). Abdomen dark brown; postcoxal line incomplete (Fig. 1N) and last ventrite emarginated (Fig. 3F).

Figure 3. 

Nephus (Geminosipho) reunioni (Fürsch, 1974) A dorsal view B ventral view C lateral view D frontal view E, F abdomen G–J male genitalia: tegmen (dorsal and lateral view): I, J penis K, L female genitalia: K spermatheca L coxites.

Genitalia with tegmen, penis guide, phallobase and parameres symmetrical. Penis guide narrow, longer than parameres, sharp at apex. Parameres articulated with phallobase, distant from each other, strongly widened at apex, with long bristles along parameres (Fig. 3G, H). Penis sclerotized, J-shaped, with projection at apex, penis capsule T-shaped and elongated (Fig. 3J, I).

Female. Length 1.75 mm, width 1.30 mm. Similar to male. Genitalia with coxites longer than wide, subtriangular, 3.0× longer than wide; stylus mamiliform with short bristles (Fig. 3L). Spermatheca short, C- shaped, without ramus and nodulus, with sharp base and truncated apex (Fig. 3K).

Material examined

Portugal: Specimens from a laboratory rearing (Laboratoire Evolution & Diversité Biologique, Université Toulouse III) initiated from field material collected in 2007 in Cascais, 10 specimens [DZUP].

Remarks

It should be noted that Fürsch (2007), in his remarks about N. reunioni, mentions “The species is referred from various authors from South Africa (det. Fürsch), and even from Israel and Portugal. These specimens are breeded for pest control, but they seem to be misidentifications and in fact N. derroni.” In what concerns the Portugal population, we do not agree with Fürsch’s statement. Indeed, the specimens collected in Portugal and analyzed in the present study correspond to the original N. reunioni description by Fürsch presented in Chazeau et al. (1974). Raimundo (1992), who first described N. reunioni for Portugal, also illustrated the external morphology and genitalia corresponding to the original description by Fürsch in Chazeau et al. (1974). In both cases, the observations show that the specimens from the Portuguese population are distinct from N. derroni, first described from S. Tomé and presented in Fürsch (1974).

Nephus (Nephus) voeltzkowi Weise, 1910

Figs 1, 4

Nephus (Nephus) voeltzkowi Weise, 1910: 512 (original description); Fürsch 2007: 6 (systematics).

Nephus seychellensis Sicard, 1912: 362 (original description); Chazeau et al. 1974: 272 (synonymy).

Scymnus (Nephus) voeltzkowi: Korschefsky 1931: 153 (catalog); Fürsch 1966: 181 (systematics).

Nephus (Nephus) voeltzkowi: Poussereau et al. 2018: 128 (systematics)

Diagnosis

Nephus voeltzkowi resembles N. oblongosignatus and N. apolonia in the color of the integument and spots but differs in the shape and size of the spots and the female genitalia.

Description

Female. Length 1.65 mm, width 1.10 mm. Body oval, with short fine whitish pubescence. Integument of pronotum, scutellar shield and elytra black. Elytra with one yellowish big oval spot on each elytron; elytra apex yellowish (Fig. 4A, C). Pronotum black, anterior border dark brown (Fig. 4A, D). Head, antennae and mouthparts light brown (Fig. 4B). Meso- and metaventrite dark brown. Epipleuron dark brown, without excavations to receive femora. Legs with coxae dark brown and femora, tibiae and tarsi light brown (Fig. 4B, D). Abdomen dark brown with two last ventrites yellowish; postcoxal line incomplete (Fig. 1O).

Figure 4. 

Nephus (Nephus) voeltzkowi Weise, 1910 A dorsal view B ventral view C lateral view D frontal view E abdomen F, G female genitalia: F coxites G spermatheca.

Genitalia. Coxites longer than wide, subtriangular, 3.0 x longer than wide; stylus mamiliform with long bristles (Fig. 4F). Spermatheca heavily sclerotized, slightly arched, striated, and marked by two strong constrictions in the middle; with sharp base and truncated apex (Fig. 4G).

Male genitalia according to Chazeau et al. (1974, plate II, figs 6, 7, 9, 10): tegmen, penis guide, phallobase and parameres symmetrical. Penis guide slightly longer than parameres. Parameres slender, articulated with phallobase, distant from each other, with bristles at apex. Penis sclerotized, J-shaped, with membranous apex, penis capsule T-shaped.

Material examined

Reunion Island: Specimens from a laboratory rearing (Laboratoire Evolution & Diversité Biologique, Université Toulouse III) initiated from field material collected in November 2011 in Manapany-les-Bains, 14 specimens [DZUP].

Remarks

It should be noted that only female specimens of N. voeltzkowi were observed here. Furthermore, although Magro et al. (2020) performed a large sampling campaign on Reunion, they never found N. voeltzkowi males, and eventually demonstrated that Reunion females are parthenogenetic. As indicated by Magro et al. (2020), the presence of N. voeltzkowi was reported before by Chazeau et al. (1974) in their fauna of ladybirds from Reunion, but the sex of the specimens was not mentioned: although Chazeau et al. (1974) presented an illustration of the genitalia of a N. voeltzkowi male, the possibility that the drawing was based on a Madagascar specimen was not discounted (Chazeau pers. com.). In the absence of the original material, we cannot confirm this information.

Nephus (Nephus) apolonia Magro & Almeida, sp. nov.

http://zoobank.org/9CCCB544-1EE3-4F28-AD13-4359F999AE33
Figs 1, 5

Diagnosis

Nephus apolonia sp. nov. is similar to N. voeltzkowi and N. oblongosignatus but differs by the size and shape of the spots and the pattern of genitalia.

Description

Male. Length 1.69 mm, width 1.2 mm. Body oval, oblong, with short fine whitish pubescence. Integument of pronotum, scutellar shield and elytra black. Elytra with one yellowish longitudinal spot on each elytron (Fig. 5A, C). Pronotum black, antero-lateral border dark brown (Fig. 5A, D). Head dark brown, antennae and mouthparts yellowish (Fig. 5B, D). Meso- and metaventrite light brown. Epipleuron light brown, without excavations to receive femora. Legs with coxae and femora dark brown, tibiae and tarsi light brown (Figs 1L, 5B, D). Abdomen light brown (Fig. 5E); postcoxal line incomplete (Fig. 1P), and last ventrite emarginate (Fig. 5F).

Figure 5. 

Nephus (Nephus) apolonia Magro & Almeida, sp. nov. A dorsal view B ventral view C lateral view D frontal view E, F abdomen G–J male genitalia: G, H penis I, J tegmen (dorsal and lateral view) K, L female genitalia: K spermatheca L coxites.

Genitalia with tegmen, penis guide, phallobase and parameres symmetrical. Penis guide shorter than parameres, sharp at apex (Fig. 5I, J). Parameres articulated with phallobase, distant from each other, strongly widened at apex, with short bristles along parameres (Fig. 5I, J). Penis sclerotized, J-shaped, with sharp apex, penis capsule T-shaped and elongated (Fig. 5G, H).

Female. Length 1.88 mm, width 1.30 mm. Similar to male. Genitalia with coxites longer than wide, subtriangular, 3.0× longer than wide; stylus mamiliform with long bristles (Fig. 5L). Spermatheca heavily sclerotized, slightly arched, not very striated, and marked by one strong constriction in the middle, with sharp base and rounded apex (Fig. 5K).

Etymology

This species is named after an early name of Reunion Island, mentioned as “Santa Apolonia” on the Portolan charts (nautical charts) from the XVIth century (GENUNG, 2017).

Type locality

Reunion Island: from a laboratory rearing (Laboratoire Evolution & Diversité Biologique, Université Toulouse III) initiated from field material collected in December 2013 in Manapany-les-Bains and Étang-Salé.

Type material

Holotype male, pinned, with genitalia in a separate microvial. Original label: “Reunion Island, 1 specimen [MNHN]”; “HOLOTYPE/ Nephus apolonia Magro and Almeida” [red label]. Paratypes. The following specimens are designated as paratypes with labels: “same data as for holotype”. “PARATYPE/ Nephus apolonia Magro and Almeida” [yellow label]: “Reunion Island, 2 specimens [MNHN, DZUP]; “Reunion Island, 1 specimen [MNHN]; “Reunion Island, 1 specimen [DZUP]; “Reunion Island, 1 specimen [MNHN]; “Reunion Island, 1 specimen [DZUP]; “Reunion Island, 2 specimens [DZUP, MNHN]; “Reunion Island, 1 specimen [DZUP].

Geographical distribution

Reunion Island: L’Étang-Salé, Le Trou d’eau (21°16'54.2"S, 55°21'39.7"E); Saint-Denis, Saint-Bernard (20°52'58.36"S, 55°23'50.19"E); Saint-Louis, Etang du Gol (21°17'20.9"S, 55°23'16.1"E); La Possession, Ravine à Malheur (20°54'03.5"S, 55°22'32.1"E); Saint-Pierre, CIRAD (21°19'13.8"S, 55°29'6"E); L’Étang-Salé, ARDA (21°17'05.6"S, 55°22'38.1"E) and Saint-Joseph, Langevin (21°22'53.4"S, 55°38'48.4"E).

Remarks

Nephus apolonia sp. nov. has apparently been misidentified as N. voeltzkowi until now. We verified that this was the case for specimens captured by the Insectarium de La Réunion. Poussereau et al. (2018) included three species for Reunion Island. In that work, N. voeltzkowi is reported with large variation and distribution. It could be possible that the specimens identified by Poussereau et al. (2018) as N. voeltzkowi included the Nephus apolonia sp. nov. described here.

Molecular analysis

The mitochondrial genome of one specimen of Nephus apolonia is deposited in Genbank under accession number MN164644. Genetic distances based on the COI sequences between N. apolonia and other Nephus species confirm that N. apolonia is different from the other species, as all distances are within the same range (i.e., 0.13–0.17) (Table 2). In the phylogenetic tree reconstructed from 14,867 pb of aligned mitochondrial genomes (Fig. 6), most nodes, including N. apolonia, were supported by high bootstrap values.

Table 2.
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Pairwise Kimura-2-parameter distances for the mitochondrial COI gene for the Nephus species.

1 2 3 4
1 Nephus apolonia
2 N. reunioni 0.131
3 N. includens 0.133 0.126
4 N. voeltzkowi 0.174 0.170 0.160
5 N. oblongosignatus 0.155 0.150 0.142 0.172
Figure 6. 

Maximum likelihood phylogeny of Nephus (Nephus) apolonia Magro & Almeida, sp. nov. and four related species based on the mitochondrial genome (without the control region) reconstructed through 1000 non-parametric bootstrap replicates. The scale bar indicates 0.04 substitutions per site. Numbers on major nodes represent Maximum Likelihood bootstrap support.

Acknowledgements

We are extremely grateful to our late colleague and friend, Serge Quilici (CIRAD, St Pierre) for his logistic support during AM visits to Reunion and more than everything for his kindness. We also would like to thank J. Rochat for access to samples from the Insectarium de La Réunion, and the Electronic Microscopy Center (UFPR) for the pictures. This study was supported by the CAPES Program “Sciences without borders” (401366/2014-6), PhD fellowship to JMCS (1578651/2016) and CNPq for the research fellowship to LMA (308992/2017-2) Brazil. Furthermore, AM, EL, and JLH were supported by the “Laboratoires d’Excellence” LabEx TULIP (ANR-10-LABX-41) and CEBA (ANR-10-LABX-25-01).

References

  • Chazeau J, Étienne J, Fürsch H (1974) Les Coccinellidae de l’île de la Réunion. Bulletin du Muséum National d’ Histoire Naturelle 3e série (210) Zoologie 140: 265–297.
  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature methods 9(8): 772–772. https://doi.org/10.1038/nmeth.2109
  • Fürsch H (1966) Die Scymnus-Arten Westafrikas (Col. Cocc.). Entomologische Arbeiten aus dem Museum G. Frey Tutzing bei München 17: 135–194.
  • Fürsch H (1974) Die Coccinelliden von São Tomé. Mitteilungen der Münchner Entomologischen Gesellschaft 64: 13–39.
  • Fürsch H (1987) Übersicht über die Genera und Subgenera der Scymnini mit besonderer Berücksichtigung der Westpalaearktis (Insecta, Coleoptera, Coccinellidae). Entomologische Abhandlungen Staatliches Museum für Tierkunde Dresden 51(4): 57–74.
  • Fürsch H (2007) Catalogue of the African species of Nephus Mulsant, 1846 with description of two new species (Coleoptera: Coccinellidae). Entomologische Zeitschrift 117(5): 1–7.
  • GENUNG (2017) Bulletin d’information toponymique. N° 10: 1–27.
  • Gordon RD (1976) The Scymnini (Coleoptera: Coccinellidae) of the United States and Canada: Key to genera and revision of Scymnus, Nephus and Diomus. Bulletin of the Buffalo Society of Natural Sciences 28: 1–362.
  • Gordon RD (1985) The Coccinellidae (Coleoptera) of America north of Mexico. Journal of the New York Entomological Society 93(1): 1–912.
  • Gordon RD, González G (2002) South American Coccinellidae (Coleoptera). Part IX: A Systematic Revision of Scymnobius Casey (Scymninae: Scymnini). Frustula Entomologica 25(38): 57–85.
  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111–120. https://doi.org/10.1007/BF01731581
  • Korschefsky R (1931) Coccinellidae I. In: Junk W, Schenkling S (Eds) Coleopterorum Catalogus, Pars 118. W. Junk, Berlin, 224 pp.
  • Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33(7): 1870–1874. https://doi.org/10.1093/molbev/msw054
  • Mader L (1924) Bestimmungs-Tabellen der Europäaischen Coleopteren. 94. Heft. Coccinellidae, Tribus Scymnini. Tropau, 48 pp.
  • Magro A, Lecompte E, Hemptinne JL, Soares AO, Dutrillaux AM, Murienne J, Fürsch H, Dutrillaux B (2020) First case of parthenogenesis in ladybirds (Coleoptera: Coccinellidae) suggests new mechanisms for the evolution of asexual reproduction. Journal of Zoological Systematics and Evolutionary Research 58(1): 194–208. https://doi.org/10.1111/jzs.12339
  • Magro A, Araujo J, Hemptinne JL (1999) Coccinellids (Coleoptera: Coccinellidae) in citrus groves in Portugal: listing and analysis of geographical distribution. Boletín de Sanidad Vegetal Plagas 25: 335–345.
  • Mulsant E (1846) Histoire Naturelle des Cóleoptères de France. Sulcicoles Sécuripalpes. Maison, Paris, 280 pp.
  • Mulsant E (1850) Species des Cóleoptères Trimères Sécuripalpes. Annales des Sciencies Physiques et Naturelles, d’Agriculture et d’Industrie, publiées par la Sociètè nationale d’Agriculture de Lyon, 1104 pp. https://doi.org/10.5962/bhl.title.8953
  • Pope RD (1957) Coccinellidae. South Animal Life. Uppsala 4: 292–322.
  • Poussereau J, Coutanceau JP, Nicolas V, Gomy Y (2018) Les coccinelles de l’île de la Réunion. Orphie, 222 pp.
  • Raimundo A (1992) Novas espécies de Scymnini para a fauna de Coccinelídeos de Portugal. Boletim da Sociedade Portuguesa de Entomologia, Sup. 3, vol. 1: 373–384.
  • Robertson JA, Ślipiński A, Moulton M, Shockley FW, Giorgi A, Lord NP, Mckenna DD, Tomaszewska W, Forrester J, Miller KB, Whiting MF, Mchugh JV (2015) Phylogeny and classification of Cucujoidea and the recognition of a new superfamily Coccinelloidea (Coleoptera: Cucujiformia). Systematic Entomology 40: 745–778. https://doi.org/10.1111/syen.12138
  • Seago AE, Giorgi JA, Li J, Ślipiński A (2011) Phylogeny, classification and evolution of ladybird beetles (Coleoptera: Coccinellidae) based on simultaneous analysis of molecular and morphological data. Molecular Phylogenetics and Evolution 60: 137–151. https://doi.org/10.1016/j.ympev.2011.03.015
  • Sicard A (1909) Revision des Coccinellides de la Faune Malgache. Annales de la Société Entomologique de France 78: 63–165.
  • Ślipiński A (2007) Australian Ladybird Beetles (Coleoptera: Coccinellidae): Their Biology and Classification. ABRS, Canberra, 286 pp.
  • Weise J (1910) Coccinellidae von Madagaskar, den Comoren und den Inseln Ostafrikas. Voeltzkow, Reise in Ostafrika in den Jahren 1903–1905 2: 507–520.
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