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Phylogeny of the Ceratocanthinae (Coleoptera: Hybosoridae)

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Phylogeny of the Ceratocanthinae (Coleoptera: Hybosoridae) ZOBODAT - www.zobodat.at Zoologisch-Botanische Datenbank/Zoological-Botanical Database Digitale Literatur/Digital Literature Zeitschrift/Journal: Arthropod Systematics and Phylogeny Jahr/Year: 2016 Band/Volume: 74 Autor(en)/Author(s): Ballerio Alberto, Grebennikov Vasily V. Artikel/Article: Rolling into a ball: phylogeny of the Ceratocanthinae (Coleoptera: Hybosoridae) inferred from adult morpho-logy and origin of a unique body enrollment coaptation in terrestrial arthropods 23-52 74 (1): 23 – 52 14.6.2016 © Senckenberg Gesellschaft für Naturforschung, 2016. Rolling into a ball: phylogeny of the Ceratocanthinae (Coleoptera: Hybosoridae) inferred from adult morpho- logy and origin of a unique body enrollment coaptation in terrestrial arthropods Alberto Ballerio 1 & Vasily V. Grebennikov 2 1 Viale Venezia 45, I-25123 Brescia, Italy; Alberto Ballerio [[email protected]] — 2 Canadian Food Inspection Agency, Ottawa Plant Laboratory, KW Neatby Bldg., 960 Carling Ave, Ottawa, Ontario K1A 0Y9, Canada; Vasily V. Grebennikov [[email protected]] Accepted 13.i.2016. Published online at www.senckenberg.de/arthropod-systematics on 03.vi.2016. Editor in charge: Joe McHugh. Abstract Results of a phylogenetic analysis of all but one of the 43 recognized extant genera of Ceratocanthinae scarab beetles (Coleoptera: Hy- bosoridae) are reported. The analysis is based on 97 parsimony informative adult morphological characters scored for 61 ingroup and 10 outgroup terminals. This pantropical subfamily of some 366 species is remarkable for the adults’ ability to pack their body into a tight sub-sphere using interlocking exoskeletal structures (= enrollment coaptations). An overview on known biological and fossil data on the subfamily is provided, as well as a list, an overview, a key and illustrations of adults of all Ceratocanthinae genera. The phylogenetic analy- sis supports a monophyletic Ceratocanthinae (bootstrap 76%) and a basal dichotomy between pantropical Ceratocanthini (97%) and the South American clade (98%) of Scarabatermitini. Ivieolini renders Scarabatermitini paraphyletic. Another well supported internal clade is the Philharmostes group of seven Afrotropical genera (85%). All other inclusive clades detected in the analysis have low bootstrap support (51–65%), likely indicative of limitations of the adult morphological dataset. We also provide a detailed distribution map of Ceratocanthi- nae and hypothesize about the South American origin of the subfamily, and that of its two subclades: Ceratocanthini and Scarabatermitini + Ivieolini. Overall this paper summarizes all existing information on Ceratocanthinae beetles in an evolutionary context in order to facilitate and stimulate further research on this subfamily. Key words Ceratocanthini, Ivieolini, Scarabatermitini, conglobation, coaptation, key to genera, distribution, fossils, biogeography. 1. Introduction Ceratocanthinae are a pantropical subfamily of Hybosori- (but not monophyly of the former) was first demonstrated dae (Coleoptera: Scarabaeoidea) comprising some 366 by GREBENNIKOV et al. (2004) using 57 larval characters described species. Most species are easily recognized from 17 Hybosoridae (of which 11 were Ceratocanthini) by the remarkable ability of the adult to form a nearly and nine outgroup terminals. OCAMPO (2006) used 117 perfect ball. This, along with some other shared similari- adult morphological characters of 40 Hybosoridae termi- ties, led to an early recognition of Ceratocanthinae as a nals (of which two were Ceratocanthini) to corroborate natural group, although for a long time it was treated as monophyly of Ceratocanthinae, as well as that of four a family distinct, but allied with, Hybosoridae. Phyloge- other extant subfamilies: Anaidinae, Hybosorinae, Lipa- netic placement of Ceratocanthinae within Hybosoridae rochrinae and Pachyplectrinae. OCAMPO & HAWKS (2006) ISSN 1863-7221 (print) | eISSN 1864-8312 (online) 23 Ballerio & Grebennikov: Ceratocanthinae phylogeny and enrollment coaptation Fig. 1. Ceratocanthinae, live beetles. A: Ceratocanthus sp., Belize; B: Eusphaeropeltis sp., China; D: Ebbrittoniella gestroi, Malaysia; C: Philharmostes sp., Madagascar; E: Madrasostes agostii, Malaysia. used a 2061 bp alignment of 28S and 18S rDNA for 36 As highlighted above, adult Ceratocanthinae are terminals, of them 20 belonging to Hybosoridae (seven best known by their ability to conglobate (Fig. 1A – E). of them being Ceratocanthini), to recover all extant Hy- This ability to roll into a tight compact structure prob- bosoridae subfamilies as monophyletic, and Ceratocan- ably has anti-predatory and physiological (moisture re- thinae forming a weakly supported clade (78% bootstrap) tention, thermoregulation) advantages. Some members with Liparochrinae. SMITH et al. (2006) extended the of the subfamily are capable of forming a subsphaerical same rDNA dataset to include 600 (28S) and 150 (18S) structure, with elytra, pronotum, head, and all six tibi- Scarabaeoidea terminals to corroborate the placement ae forming a tightly connected external surface. These of Ceratocanthinae within Hybosoridae. The subfamily structures interlock with each other by means of grooves comprises three tribes (HOWDEN & GILL 2000): Cerato- and corresponding ridges. The degree of mechanical co- canthini, Ivieolini and Scarabatermitini, whose mono- aptation is so high, that unrolling a dead Ceratocanthini phyly and interrelationships have never been cladisti- specimen requires significant practice and some under- cally tested. The former includes 38 genera and > 95% of standing of the body mechanics. Other Ceratocanthini the extant species, while the latter two are comprised of species are less morphologically committed, although five genera and eight bizarre species restricted to South they can still have their head and pronotum markedly de- America. flexed in a similar manner to three other Coleoptera line- 24 ARTHROPOD SYSTEMATICS & PHYLOGENY — 74 (1) 2016 ages exhibiting parallel morphological adaptations. This Very little is known about Ceratocanthinae life his- ball-forming capacity among the non-Ceratocanthini tory and immature stages. Larvae are markedly elongate beetles is restricted, however, to bending the pronotum and have been described for representatives of seven and head in the ventral direction and pressing the ventral genera (GREBENNIKOV et al. 2004). Larvae were collected side of the latter against the meso- (Cybocephalidae) and together with adults in termite nests (Pterorthochaetes, metathorax (Clambidae, Leiodidae: Agathidium Panzer, Cyphopisthes, Paulianostes and Madrasostes) and un- 1797), thus leaving at least some apical abdominal seg- der bark (Pterorthochaetes). Pupae of some species ments partly exposed. Moreover, in Ceratocanthinae, the have support projections (GREBENNIKOV et al. 2002), tibiae of all six legs participate in forming the external which suggest the existence of a pupal cell. Adults of hard surface of the sphere, unlike in other beetles. The many species of Ceratocanthinae are found in termite very different, and perhaps no less weirdly shaped, Ivieo- nests. Scarabatermitini (and probably Ivieolini) seem to lini and Scarabatermitini are incapable of deflexing their be adapted to life with termites such as Neocapritermes body, let alone forming a tight ball. This could be a re- Holmgren, 1912, Cornitermes Holmgren, 1906 and Pro­ versal, since some non-Ceratocanthinae members of Hy- cornitermes Emerson, 1949, which involves the devel- bosoridae (e.g., Liparochrus) have at least some capacity opment of several morphological traits like physogastry of body deflexion. and depigmentation (SILVESTRI 1940; HOWDEN 1973). The subfamily Ceratocanthinae has a mainly pan- Possible termitophily of Ceratocanthini is, however, not tropical distribution (Fig. 2), with only a few genera and well understood or corroborated with data. The capabil- species recorded from the adjacent parts of the northern ity to roll the body into a sphere has possible defensive and southern temperate regions (OCAMPO & BALLERIO purposes and might have evolved to support a lifestyle in 2006 and unpublished data). The subfamily is particular- the hostile environment of a termite nest. Several records ly diverse in the New World with 16 genera and at least of Ceratocanthini species found in termite nests of Cop­ 170 species recorded from Chile to Canada. Only three totermes Banks, 1919, Dicuspiditermes Krishna, 1965, species occur north of Mexico, mainly in eastern North Hospitalitermes Holmgren, 1912, Mastotermes Frog- America, with their distributions extending west to west- gatt, 1897 and Nasutitermes Dudley, 1890 (BALLERIO & ern Nebraska and north to Ontario. Many species occur MARUYAMA 2010; IWATA et al. 1992; PAULIAN 1977, 1978) in Central America (including the Caribbean, where the do not provide indications of the exact kind of relation- endemic genus Nesopalla is found) and in South Amer- ship between the beetles and termites. IWATA et al. (1992) ica, south to northern Argentina. Chile and the Valdiv- suggested that the beetles might be termitariophilous, i.e. ian temperate forests that intrude into Argentina have the attracted to termite nests. This hypothesis is further cor- endemic genus Martinezostes and the likely congeneric roborated by the observation of Astaenomoechus species “Germarostes” posticus (Germar, 1843). Ceratocanthi- seemingly being attracted to fragments of arboreal ter- nae are abundant in suitable habitats in the Afrotropical
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