Phylogenetic relationships of the genus Hoplia Illiger (Scarabaeidae: Hopliinae)

SYSTEMATICS, MORPHOLOGY AND PHYSIOLOGY

Phylogenetic relationships of the genus Hoplia Illiger (Scarabaeidae: Hopliinae)

H Carrillo-Ruiz^I; MA Morón^II

^IEscuela de Biología, Benemérita Univ Autónoma de Puebla, Blvd Valsequillo y Av San Claudio, Ciudad Universitaria, Puebla, México

^IIRed de Biodiversidad y Sistemática, Instituto de Ecología A. C., Xalapa, Veracruz, México

^{Correspondence}

ABSTRACT

Results of phylogenetic analysis based on 34 morphological characters of 24 species of 11 genera of Hopliinae from Europe, Japan, South Africa, Madagascar, North and Central America, indicates that the genus Hoplia is a monophyletic group with species distributed in Europe, Japan and America. Based in this analysis the Asiatic genus Ectinohoplia is the closest relative of the genus Hoplia, and the South American genus Barybas (Melolonthinae: Macrodactylini) is the sister group of Hopliinae.

Keywords: Phylogenetic hypothesis, morphological character

Introduction

The genus Hoplia Illiger is one of 62 genera belonging to the subfamily Hopliinae (Carrillo-Ruiz & Morón 2006). Most part of the species richness of the group belongs to this genus, including 297 of 397 species of the hopliids in the world (Dalla-Torre 1912-1913, Boyer 1940, Hardy 1977, Lacroix 1998, Micó 2001). Species of Hoplia are widely distributed in the Middle East, Asia, Europe, Northern Africa and Madagascar, as well as in America North of Panamá (Dalla-Torre 1912-13, Hardy 1977, Baraud 1981, Lacroix 1998, Evans 2003, Micó et al 2003). The type species of the genus is Scarabaeus farinosus L., subsequently designated by Medvedev in 1952 (Evans 2003), includes small species (0.4-0.7 mm) that are characterized by the wide body, slightly depressed and covered with abundant scales and setae. The clypeus is short and the antennal club is usually short and oval. Pygidium protrudes at the end of the elytra, without apical spurs of metatibia and a single metatarsal claw (Morón et al 1997).

Little is known about the biology of the species of this genus. Ritcher (1949) described the larvae of three North American species: Hoplia equina LeConte, H. oregona LeConte and H. cazieri Boyer (but following Evans (2003) the last two names were synonymized under H. callipyge LeConte). The adults of Hoplia sackeni LeConte and H. callipyge have been observed feeding on foliage and flowers (Boyer 1940) and adults of H. squamifera Burmeister occasionally have been collected on flowers of Hibiscus rosa-sinensis (Morón 1996). Adults of the Iberian species of Hoplia feed mainly on pollen of Gramineae, Rosaceae, Plantaginaceae, Asteraceae, Malvaceae, Umbeliferae and numerous fruit trees (Micó 2001).

Available publications on the genera of Hopliinae mainly are regional works on taxonomy (Péringuey 1902, Boyer 1940, Baraud 1981, Lacroix 1998, Hardy 1977, Micó et al 2003), but works on the phylogenetic relationships of these genera are scarce (Carrillo-Ruiz & Morón 2006). The objectives of the present study were: a) to confirm the monophyly of the American species of hopliids and their inclusion into the genus Hoplia; b) to obtain a hypothesis of the phylogenetic relationships among some species of the genus Hoplia distributed in Asia, Europe and America, with representative species of the genera Madahoplia Lacroix, Odontoplia Fairmaire, Echyra Erichson, Gymnoloma Burmeister, Hoplocnemis Harold, Peritrichia Burmeister, Lepithrix Serville, Heterochelus Burmeister and Scelophysa Burmeister (Hopliinae), distributed in South Africa and Madagascar.

Material and Methods

Taxa selection

In this study, we selected taxa based on the hypothesis proposed by Carrillo-Ruiz & Morón (2006), in which hopliids are considered a subfamily of the Scarabaeidae. The out-group was formed with representative species of five genera of Melolonthinae (Melolonthini and Macrodactylini). The in-group was formed with 24 representative species of 11 genera of Hopliinae (Table 1). We studied 160 males deposited in the collections of Instituto de Ecología A. C., Xalapa (IEXA), Canadian National Collection, Ottawa (CNC), University of Nebraska State Museum, Lincoln (UNSM), National Museum of Natural History, Washington D. C. (NMNH), The Natural History Museum, London (NHML), and the private collections of M. A. Morón, Xalapa, México (MXAL), H. F. Howden (HAHC), and Bruce Gill (BDGC) Ottawa, Canada. Also we examined the type material of Hoplia argyritis Bates, Hoplia asperula Bates and Hoplia surata Bates. Dried specimens were softened with water vapor in order to dissect the genitalia and mouthparts. These structures were extracted using microforceps and insect pins, card-mounted, and then pinned beneath each specimen. The left elytron were separated to treat with KOH (5%) and then dry-mounted for scanning with an electron microscope (Jeol JSM-5600LV, 1,000x to 2,000x), to obtain better definition of the morphology of the setae and scales. We then proceeded to score each of the 34 morphological characters (See Online Supplementary Material - ^{Appendix 1}).

Phylogenetic methods

Phylogenetic analyses were performed using 34 morphological characters. The matrix of characters employed for the analysis (Table 2) was built and analyzed using Winclada ver. 1.00.08 (Nixon 2002) and NONA ver. 2.0 (Goloboff 1999). The data were analized with a heuristics search routine (1,000 replications). Characters states for the cladistic analysis were polarized by out-group comparison (Maddison et al 1984, Nixon & Carpenter 1993). Characters are scored only for males, and all the characters were discrete rather than continuous values. Characters were coded as either binary or multistate (0-4). Multistate characters were treated as unorderer and with equal weight. The tree was rooted with the Melolonthinae, Phyllophaga lenis Horn. To evaluate the characters of the matrix we obtain the bootstrap values (1000 replications).

Results and Discussion

The phylogenetic analysis resulted in five equally parsimonius trees with a total length (TL) of 159, consistency index (CI) of 0.410, and retention index (RI) of 0.71. The strict consensus tree is shown in the Fig 1. In this phylogenetic hypothesis, two main clades were obtained. The first clade (1), including three representative species of Macrodactylini (Ceraspis pilatei Harold, Isonychus ocellatus Burmeister and Macrodactylus sylphis Bates), is supported by a bootstrap value of 63% and two synapomorphies: sixth abdominal sternite well development and disc of the mentum furrowed.

The relationships among Isonychus ocellatus and Macrodactylus sylphis (clade 3) is supported by three synapomorphies: short, abundant, piliform setae at the pronotum, protibia with two well- defined teeth and distal part of left mandible truncated.

The second main clade (2), support the relationships among Barybas aurita Bates and the clade 4, joins all the representative species of Hopliinae. The clade 2 is supported by a bootstrap value of 60% and two synapomorphies: oval squamiform setae on elytra and one metatibial spur.

The clade of the Hopliinae (4) is supported by a bootstrap value of 71% and five synapomorphies: one metatarsal claw (character state that changes in Dichelus detritus Burmeister and in Scelophysa pruinosa Burmeister), widely retractile metatarsal claws, metatarsal claws without onychia, basis of the spiculum gastrale truncated and distal part of left mandible truncated. The Madagascar species Madahoplia nodipennis (Burmeister) is related with the clade 5 that maintains the relationships of the rest of the Hopliinae and is supported by one synapomorphy: basis of the spiculum gastrale widened. Two species from Madagascar appears closely related Echyra oberthuri Lacroix and Odontoplia alluandi Fairmaire (clade 6), this relationship is supported by three synapomorphies: lateral edge of the pronotum entire, protibia with two well defined teeth and mesocoxae separated.

The clade 7 joins South African genera and the clade (9) that maintains the relationships among the representative species of the genus Ectinoplia and the representative species of the genus Hoplia is supported by a bootstrap value of 51% and three synapomorphies: clypeal apex rounded, posterior edge of pronotum with piliform setae and metatibial external border entire.

The clade of the six South African species (clade 8) is supported by a bootstrap value of 60% and two synapomorphies: body depressed and pronotum with large, abundant piliform setae. The clade of Hoplocnemis mutica Burmeister, Peritrichia vansoni Schein, Lepithrix fulvipes Thunberg, D. detritus and S. pruinosa (clade 10) is supported by a bootstrap value of 52% and two synapomorphies: clypeal apex ornate and mesoepimera dorsally exposed. The relationships of D. detritus, S. pruinosa, Peritrichia vansoni and L. fulvipes (clade 12) is supported by two synapomorphies: protibia with apical spurs and apex of the parameres acute.

Ectinohoplia obducta Motschulsky appears as the sister taxon of the genus Hoplia (clade 9), is supported by a bootstrap value of 53% and three synapomorphies: metatibiae without spurs, short distance between the protibial teeth and parameres large. The relationships among all species of Hoplia (clade 11) are supported by a bootstrap value of 61% and two synapomorphies: anterior clypeal apex entire and pronotum with short, scarce, piliform setae and distal part of the left mandible curved.

The clade of the genus Hoplia is formed by two main clades: the first, clade 13 that maintains the relationships among European and Asiatic species [Hoplia moerens Waterhouse, H. pollinosa Kryn, H. farinosa (L.), H. clorophana Erichson and H. coerulea (Drury)], is supported by two synapomorphies: short clypeus and apex of the spiculum gastrale rounded, the relationships among Euro-asiatic species are not resolved at all; we obtained a polytomy among H. pollinosa, H. farinosa, H. clorophana and Hoplia coerulea, species with rounded squamiform setae without stalk.

The second, clade 14 joins the North American species (H. dispar LeConte, H. trivialis Harold, Hoplia equina LeConte and H. modesta Haldeman) and North and Central American species is supported by two synapomorphies: metatibial external border sinuate and without frontoclypeal suture.

The clade of the Hoplia species from the United States and Canada (clade 16) is supported by one sinapomorphy: distance between the protibial teeth large. In this clade H. equina and H. modesta are very closely related, the two species present the external metatarsal claw cleft.

The clade joining the species of North and Central America (clade 17), is supported by one synapomorphy: ten antennal segments. In this clade two species are very close, H. argyritis and H. asperula, the relationship is supported by two synapomorphies: monochromatic antenna and apex of the parameres with piliform setae.

With our analysis the monophyly of Hopliinae is not rejected; the species of Barybas is the closest relatives of the hopliids, in fact Barybas is the sister group of the Hopliinae, these results are congruent with the phylogenetic hypothesis proposed by Carrillo-Ruiz & Morón (2006).

This phylogenetic hypothesis supports the genus Hoplia closely related to the species of the genus Ectinohoplia as it sister group. Both genera present the metatibiae without spurs, however in the genus Hoplia the distal part of the left mandible is curved while in Ectinoplia the distal part of the left mandible is shortened; moreover in all species of Hoplia the clypeal apex is entire and in the species of Ectinohoplia represented in this study the clypeal apex is sinuate.

The results obtained in this work show the Madagascaran genera as paraphyletic group with a basal position in the topology with respect to the others hoplines. It is possible that the species distributed in Madagascar constitute the sister group of the subfamily Hopliinae and perhaps its position is out of this subfamily (Lacroix 1998). By the other hand this hypothesis maintains the South African genera very close to the Hopliinae genera distributed in Asia (Ectinoplia) and the representative species of the genus Hoplia. There is evidence that the genus Hoplia is a Holarctic group and is necessary to continue exploring the relationships among the genus Hoplia, other species of the genus Ectinoplia, and other genera of the subfamily to confirm the internal relationships of the Hopliinae.

Based on the present analysis we confirm that: a) the American species of hopliids belong to the genus Hoplia; b) the monophyly of the genus Hoplia is not rejected; c) Ectinohoplia is the closest relative of the genus Hoplia.

Acknowledgments

We thank Bruce Gill (Canada Deparment of Agriculture), Henry Howden and Francois Genier (Canadian Museum of Nature) and CaNaCol Foundation for their valuable aid and support while studying the collections in Ottawa. Mary Liz Jameson and Brett C. Ratcliffe (UNSM) for their support for studying collections conserved in Nebraska, as well as the loan of types species of Hoplia described by H. W. Bates that were deposited in London (NHML). Angel Solís (INBIO) for the loan of Hoplia specimens of Central-America. Tiburcio Laez Aponte (INECOL) obtained the scanning electron microscope images. This paper is a contribution to the research line "Coleoptera Lamelicornios de América Latina" supported by Instituto de Ecología (account 902-08-011) and a contribution to the research proyect "Sistemática y Biogeografía del género Hoplia" supported by PROMEP (account 103.5/09/7139).

Received 17 April 2010 and accepted 27 August 2010

Edited by Roberto A Zucchi - ESALQ/USP

Carrillo-Ruiz H; Morón MA (2011) Phylogenetic Relationships of the Genus Hoplia Illiger (Scarabaeidae: Hopliinae)

List of the characters used for the phylogenetic analysis. Number in parentheses indicate the state assigned for each character.

1. Body form, determined as the total length measured from the apex of clypeus to the apex of elytra divided among the maximum elytral width. Rounded (0) (two times longer than wide), elongate (1) (three times longer than wide)

2. Dorso-ventral body shape. Depressed (0), not depressed (1)

3. Proportions of the clypeus. Short (0) (wider than long), large (1) (longer than wide)

4. Clypeal apex. Rounded (0), sinuate (1), entire (2), ornate (3)

5. Anterior region of the clypeal surface. Not raised (0) (Fig 2), raised (1) (Fig 3)

6. Frontoclypeal suture. Complete-entire (0), complete-sinuate (1), printed only at sides (1), absent (2)

7. Coloration of the antenna. Monochromatic (0), dichromatic (1)

8. Number of the antennal segments. 8 (0), 9 (1), 10 (2)

9. Posterior edge of the pronotum. Without piliform setae (0), with piliform setae (1), with piliform setae only at sides

10. Squamiform setae at the pronotum. Only squamiform setae (0), only piliform setae (1), piliform and squamiform setae (2)

11. Piliform setae at the pronotum. Short-abundant (0), short-scarce (1), large-abundant (2), large-scarce (3), absent (4)

12. Lateral edge of pronotum. Entire (0), crenate (1)

13. Mesoepimera. Dorsally exposed (0), not dorsally exposed (1)

14. Squamiform setae on elytra. Large and narrow (0) (Figs 10, 15), Oval (1) (Figs 11,13), rounded (2) (Figs 12-14), absent (3)

15. Insertion of the squamiform setae at the elytral surface. With stalk (0) (Figs 13, 15), without stalk (1) (Fig 14), not apply (2)

16. Sixth abdominal sternite. Reduced (0), Well development (1)

17. Length of fifth abdominal sternite two times longer than preceeding. Absent (0), present (1)

18. Number of well defined teeth on protibial external border. 2 (0), 3 (1)

19. Apical spurs of protibiae. Absent (0), present (1)

20. Distance among the first protibial teeth and the second protibial teeth: Small (0) (less or same to 0.04 mm), large (1) (more than 0.04 mm)

21. Mesocoxae. Not separated (0), separated (1)

22. Metatibial external border. Entire (0) (Fig 4), sinuate (1) (Fig 5), curve (2) (Fig 6)

23. Metatibial spurs. Absent (0), 1(1), 2 (2)

24. Number of metatarsal claws. 1(0), 2 (1)

25. External metatarsal claw. Entire (0), cleft (1)

26. Movement of metatarsal claws. Widely retractile (0), scarcely retractile or moveless (1)

27. Metatarsal onychia. Absent (0), present (1)

28. Length of parameres. Short (0) (less length than the genital capsule), large (1) (more length than the genital capsule)

29. Apex of the parameres. Rounded (0) (Fig 7), capitate (1) (Fig 8), acute (2) (Fig 9)

30. Piliform setae on the apex of parameres. Absent (0), present (1)

31. Basis of the spiculum gastrale. Narrowed (0), widened (1), absent (2)

32. Form of the basis of the spiculum gastrale. Rounded (0), truncate (1), not apply (2)

33. Form of distal part of left mandible. Truncate (0), Curved (1), elongated (2)

34. Disc of mentum. Longitudinally without furrow (0), furrowed (1)

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Appendix 1

Publication Dates

• Publication in this collection
  09 May 2011
• Date of issue
  Apr 2011

History

• Received
  17 Apr 2010
• Accepted
  27 Aug 2010