Morphology of mouthparts poorly resolves the phylogeny of Sericini chafers (Coleoptera: Scarabaeidae)

Zoologischer Anzeiger 284 (2020) 53e65

Contents lists available at ScienceDirect

Zoologischer Anzeiger journal homepage: www.elsevier.com/locate/jcz

Research paper

Morphology of mouthparts poorly resolves the phylogeny of Sericini chafers (Coleoptera: Scarabaeidae) Jujina Frings a, Paul K. Lago b, Dirk Ahrens a, * a b

Zoologisches Forschungsmuseum A. Koenig, Adenauerallee 160, 53113, Bonn, Germany Department of Biology, University of Mississippi, University, MS 38677, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 8 August 2019 Received in revised form 23 November 2019 Accepted 23 November 2019 Available online 3 December 2019

Morphological homogeneity within Sericini has resulted in great difficulties with respect to generic classification primarily due to lack of diagnostic characters and significant levels of homoplasy of many traits used to establish and diagnose generic groups. Recently, new morphological structures have been studied within sericines to determine their systematic utility. Reported here are the results of a comparative study of sericine mouthparts. The data gathered was used to reconstruct a phylogenetic tree using parsimony analysis exclusively based on mouthpart morphology. For this study, we examined 52 morphological characters from adults of 81 currently recognized subgenera and genera. Across all species examined, the labium and the mandibular molar lobe were highly sclerotized. The different mouthparts compared among the genera were rather homogeneous and little differentiated. This may be due to the similar polyphagous-herbivore feeding behaviour common to all Sericini. The phylogenetic tree resulting from our analysis showed little resolution and did not confirm the monophyly of the two subtribes Sericina and Trochalina, but also not that of the Sericini itself. Nevertheless, we hope the extended data matrix will prove very useful when used in concert with other morphological traits to bring more clarity to the systematics and classification of Sericini. © 2019 Published by Elsevier GmbH.

Corresponding Editor: Sven Bradler Keywords: Beetles Morphology Mouthparts Phylogeny Scarabaeoidea Melolonthinae

1. Introduction The diversity of mouthparts in insects, and particularly in Coleoptera, is tremendous (Labandeira 1997; Krenn et al. 2005; Krenn 2007). Certainly, much of this variation relates to adaptations to different types of food, but differentiation of the mouthparts between larval and adult stages could be another source. Because mouthparts are composed of a set of homologous components, which are themselves highly variable, they may provide an excellent data base for phylogenetic studies and have been rather intensively studied for this purpose (Krenn 2007), but have also been used in analyses of functional and ecological morphology (Karolyi et al. 2012; Blanke et al. 2015; Karolyi et al. 2016). Beetle mouthparts, whether larval or adult, belong to the biting and chewing type and thus their groundplan consists of a pair of well developed and sclerotized mandibles and maxillae, a labrum and a labium (þepipharynx) (Krenn 2007). Mouthparts of scarab

* Corresponding author. E-mail addresses: [email protected] (P.K. Lago), [email protected], [email protected] (D. Ahrens). https://doi.org/10.1016/j.jcz.2019.11.008 0044-5231/© 2019 Published by Elsevier GmbH.

beetles (Coleoptera: Scarabaeoidea) show the same basic components (Mathur et al. 1958), and generally show strong modifictions in relation to the consistency of their food (Nel and De Villiers 1988 Nel & Scholtz 1990). In the case of “hard” or fibrous foods, these modifications usually take the form of reductions, and often fusion of single components, particularly in many modern phytophagous lineages (e.g., Ahrens 2006c). In the present study, we investigated the phylogenetic relationships within the tribe Sericini based on comparative morphology of their mouthparts. Sericini (sensu Dalla Torre 1912) is part of the pleurostict branch of Scarabaeidae (Erichson 1847), a monophyletic lineage, which includes the major chafer subfamilies such as Dynastinae (rhinoceros beetles), Rutelinae, Melolonthinae, Cetoniinae and several other smaller groups (Ahrens & Vogler 2008) and whose members are mainly phytophagous. Currently, Sericini are placed in the subfamily Melolonthinae; however, several recent studies have shown that Melolonthinae are not a monophyletic group but a paraphyletic assemblage of various lineages (e.g., Ahrens et al. 2011). With nearly 4000 described species in about 200 genera, Sericini is very species rich (Ahrens & Vogler 2008). However, despite some recent, very detailed studies of their

54

J. Frings et al. / Zoologischer Anzeiger 284 (2020) 53e65

phylogeny (Ahrens 2006c; Ahrens & Vogler 2008; Ahrens et al. 2011; Liu et al. 2015) and taxonomy (e.g., Fabrizi & Ahrens 2014; Ahrens & Fabrizi 2016), for most species our knowledge concerning taxonomy and classification is quite limited. All papers examining the phylogenetic relationships within the tribe (Ahrens 2006c; Ahrens & Vogler 2008) have reported monophyly of the tribe, which is supported by a large number of morphological synapomorphies (Ahrens 2006c), and Ablaberini were identified as sister group of the Sericini (Ahrens 2006c; Ahrens & Vogler 2008; Ahrens et al. 2011; Liu et al. 2015). Sericini are most diverse in tropical and subtropical zones, but are also well represented in the Holarctic (except in the polar and subpolar region). However, they are entirely absent in New Guinea, Australia, New Zealand and southern South America (Ahrens 2006c). They are generalist herbivores (Ahrens 2006c). As is true for other Melolonthinae, adults feed on leaves of angiosperm plants and larvae feed on roots (Ahrens & Vogler 2008). Many Sericini are nocturnal and are inconspicuously colored, generally being various shades of brown, which adds to the difficulty of species determinations. Mouthpart morphology in scarab beetles has been used in various studies for various purposes (Williams 1938; Mathur et al. 1958; Machatschke 1959; Nel & De Villiers 1988; Scholtz 1990; Nel & Scholtz 1990; Hayes 1992; Beutel 1994; Betz et al. 2003; Anton & Beutel 2004, 2012; Philips et al. 2004; Wilhelmi & Krenn 2005; Krenn et al. 2005; Ahrens 2006a,b,c; Ball et al. 2011; Li et al. 2013; Bai et al. 2015; Karolyi et al. 2016). Among these studies, few have been conducted for phylogenetic reconstructions, and those that did generally used mouthparts in combination with other traits (Williams 1938; Hansen 1991; Sanmartín & Martín-Piera 2003; Ahrens 2006c; Cabrero-Sanudo 2007). Fewer still considered comparative morphology and relationships within Sericini (Machatschke 1959; Ahrens 2006c). Morphological homogeneity of sericines has resulted in difficulties in generic classification (Ahrens 2004) due to lack of diagnostic characters and significant homoplasy of many traits used in the past to establish and diagnose generic groups (Ahrens & Vogler 2008; Liu et al. 2015). Recently, explorations have begun to find new morphological traits and to assess their suitability for sys€ tematic analyses (Kastenholz and Ahrens, unpublished data; OzgülSiemund & Ahrens 2015). Mouthparts of Sericini have not been comprehensively studied. Traditionally, the fusion of labrum with the clypeus was considered to be one of the key characters of Sericini (Burmeister 1855; Machatschke 1959), thus some mouth part features were incorporated into traditional classification of the group (e.g., Burmeister 1855; Reitter 1902; Machatschke 1959). A few characters of the maxilla and the labium have been used for phylogenetic analysis (Ahrens 2006c), but these data were rather limited and did not include the mandibles, labrum or epipharynx. In this study, comparative morphology of the mouthparts for a wide range of sericine genera (n ¼ 81) is investigated, and these are compared to the mouthparts of related lineages (e.g., Ablaberini (Cyrtocamenta Brenske, 1897 sp.) and two other melolonthine tribes (Heteronyx rin-Me neville, 1831 sp. (Heteronycini) and Sparrmannia CasGue telnau, 1840 sp. (“Melolonthinae")). The comparative data subsequently was used to explore the phylogenetic information content of these characters and, using parsimony analysis, a phylogenetic tree was constructed based on mouthpart morphology exclusively. 2. Material and methods 2.1. Taxon sampling For this study, 81 genera and subgenera of Sericini were examined, which represents nearly 70% of the extant and currently

available genus group names of Sericini. For each of the 125 species examined, we studied and documented at least two specimens (Supplement Table 1). We used the type species of each genus whenever possible (Ahrens 2007a, b). As outgroup taxa (all Melolonthinae), we chose Cyrtocamenta sp. (Ablaberini), Sparrmannia sp. (Melolonthini), Diphucephala Dejean, 1821 sp. (Diphucephalini) and Heteronyx sp. (Heteronychini), the latter three closely related to Sericini, and Ablaberini (Ahrens & Vogler 2008; Ahrens et al. 2014). The resulting trees were rooted with Sparrmannia. All specimens examined originated from the collection of the Zoologisches Forschungsmuseum Alexander Koenig, Bonn (ZFMK). 2.2. Preparation of mouthparts and data gathering Dried collection specimens were softened in water (distilled or deionized) with a few drops of surfactant over a 12e24 h period (Dellacasa et al. 2010). To accelerate the softening process, dried specimens were relaxed in hot distilled water for several minutes. The mouthparts of the softened specimen were then dissected: the labium, two maxillae and two mandibles were removed from the head using sharply pointed forceps. The mouthparts were dehydrated in a series of 70%, 80%, 90% and 100% ethanol, each step for 10 min respectively. Finally, they were washed with acetone once and were cleaned for about 5e10 s in an ultrasonic cleaner (Emmi 30). The duration of this step depended on the sclerotization (i.e., the risk of damage) and the contamination of the mouthparts. For example, mandibles could be cleaned longer in an ultrasonic cleaner than a labium or a maxilla. The structures were then dried on a glass slide and mounted on a 0.5-inch aluminium specimen stub using a conductive adhesive. Specimens were coated with a thin layer of electrically conducting metal (gold) by low vacuum sputter coating (Cressington coating systems; Cressington 108 auto). Images were taken with a scanning electron microscope Hitachi S-2460N. The labium and labrum were imaged ventrally, while maxilla and mandible images were taken from ventral and dorsal view, the latter additionally from mesal (internal) view, to illustrate the precise morphology of the molar lobe. The comparative analysis of the mouthparts revealed 52 useful characters, specifically four characters for the labium, nineteen for the maxillae, nine for the labrum/epipharynx, and twenty for the mandible. General character terminology followed Ahrens (2006c) (Figs. 1 and 2, Table 1). We refrained from character state descriptions and from formulating any hypothesis about their transformations. In particular, coding is not implying whether a state is derived or ancestral. The data matrix is presented in Table 2. 2.3. Phylogenetic analysis All 52 characters were run unordered, nonadditive, and equally weighted. Inapplicable character states were scored as "-" and unknown character states were scored as "?" (Strong & Lipscomb 1999). The parsimony analysis was performed in NONA 2.0 (Goloboff 1999; Nixon 2002) using the parsimony ratchet (Nixon 1999) implemented in NONA and run in WINCLADA version 1.00.08 as a shell program (Nixon 2002). In a first run, two hundred iterations were performed (one tree hold per iteration), with the number of characters to be sampled for reweighting during the parsimony ratchet determined to be ten. Subsequently, each analysis was repeated 10 times in order to detect shorter trees. All searches were run under the collapsing option ‘ambiguous’, which collapses every node whose minimum length is 0. State transformations were considered to be apomorphies of a given node only if they were unambiguous (i.e., without arbitrary

J. Frings et al. / Zoologischer Anzeiger 284 (2020) 53e65

55

Fig. 1. Labium (A, Comaserica bergrothi; B, Hellaserica elongata; C, Pleophylla fasciatipennis; D, Astaena sp.); E, maxilla, ventral view, Diphucephala sp.; maxilla, dorsal view (F, Omalopia erythroptera; G, Hymenoplia castilliana; H, Allokotarsa sp2 _; I, Sparrmannia sp.; J, Heteronyx sp.; K, Triodontella aquilla; L, Pleophylla fasciatipennis); lacinia (M, Hyboserica alexandriana; N, Paratriodonta romana; O, Cyrtocamenta sp.; P, Astaena sp.; Q, Hyposerica cruciata; R, Ablaberoides moestus; S, Maladera clypeata; T, Heteronyx sp.; U, Pleophylla fascitiapennis); epipharynx/labrum (V, Diphucephala sp.; W, Symmela pallipes; X, Glaphyserica humeralis). See Table 1 for explanation of abbreviations.

56

J. Frings et al. / Zoologischer Anzeiger 284 (2020) 53e65

Fig. 2. Epipharynx/labrum (A, Ablaberoides moestus; B, Amiserica flavolucida; C, Plotopuserica darwiniana; D, Astaena sp., E, Camentoserica livida); mandible, dorsal view (F, Cyrtocamenta sp.; G, Triodontella aquila; H, Bilga sp.); Mandible ventral view (I, Sparrmannia sp.; J, Triodontella aquila; K, Astaena sp.; L, Diphucephala sp.; M, Arraphytarsa sp. \; N, Cyrtocamenta sp.; O, Phylloserica sp.; P, Trichomaladera yui; Q, Heteroserica hovana); Mandible ventral-internal view (R, Arraphytarsa sp. \; S, Cyrtocamenta sp., T, Euronycha rhodisiana; U, Paratriodonta romana; V, Pseudosericania makiharai; W, Omalopia nigromarginata; X, Selaserica nitida). See Table 1 for explanation of abbreviations.

J. Frings et al. / Zoologischer Anzeiger 284 (2020) 53e65 Table 1 Abbreviations used for the terminology of morphological character descriptions. actp ap bcml bs bst ca-l cd chtp con dpmst dta dtaml ggl gl hl iph lbm lbr lc ll lo-ml lb lsc mdb msbr msp mst mt mx-l mx-r pe-ms pf pg pmx prmt sbm s-e s-i Ss

acanthoparie apicalis basal carina of molar lobe basalis basistipes callum laterale (of laterale sclerite) cardo chaetopariae condylus dorsal process of medial stipes distal tooth of apicalis distal tooth of area of molar lobe ginglymus galea heli ipophobae labium lacinial brush lacinia ligular lobe lobus molaris labial palp lateral sclerite mandibular brush mesal brush mesophoba mediostipes mentum left maxilla right maxilla pectineus medialis palpifer palpiger palpi maxilliares prementum submentum sutura externa of callum laterale sutura interna of callum laterale sensillum

57

the cardo (cd), stipes (composed of basistipes (bs) and mediostipes (mst)), lacinia (lc), galea (gl), palpifer (pf) and maxillary palpus (pmx) (Williams 1938). Most of the species have a galea with a ventral and a dorsal row of teeth that are well separated (Fig. 1F), and some have fused teeth on the ventral distal region as in Hymenoplia castilliana Reitter, 1890 (Fig. 1G). The number of teeth present on each galea varies from five to eight. All the species have a four-jointed maxillary palpus, with the distal maxillary palpomere being largest. Most of the species examined have the maxillary palpus distinctly shorter than the length of maxilla (excluding galea), except for a few species (e.g., Allokotarsa Peringuey, 1904 sp. (Fig. 1H), Plotopuserica darwiniana Brenske, 1900). The distal joint of labial and maxillary palpi generally has a fine brush of sensillae. Apart from Diphucephala sp. (outgroup), Phylloserica Brenske, 1899 sp., Pleophylla fasciatipennis (Blanchard, 1850) (Fig. 1L) and members of the genus Omaloplia Schoenherr, 1817, all the other species have the lacinia as long as or slightly longer or slightly shorter than the galea length. The apex of the lacinia is convexly rounded in most species of Sericini. This is the case in all species of Maladera Mulsant & Rey, 1871 (Fig. 1S, Maladera clypeata (Fairmaire, 1887), except for Maladera marginella (Hope, 1831) which has a nearly truncate apex. The paired mandibles are situated ventral to the epipharynx and fit precisely against the latter. Mandibles are complex structures with a wide membranous pectineus medialis, except in the outgroup Sparrmannia sp., with a variable but usually strongly sclerotized molar lobe. The number of rows of teeth on the molar lobe varies considerably: no teeth are present in Cyrtocamenta sp. (Ablaberini) (Fig. 2S), some Sericini species have four or fewer rows of teeth, and others have more than nine rows of teeth. In many cases, portions of the molar lobe lack teeth or rows of teeth. The unarmed areas may encompass the entire basal portion of the molar lobe, the basidorsal portion (e.g., Omalopia nigromarginata (Herbst, 1785) Fig. 2W) or, as in Pseudosericania makiharai Hirasawa, 1991 (Fig. 2V), the basiventral portion. 3.2. Characters and character states

selection of accelerated or delayed optimization) and if they were shared by all dichotomized most-parsimonious trees.

3. Results 3.1. General mouthpart morphology For the most part, male specimens were used during this study. A few females were included to investigate apparent sexual dimorphism: in some cases, the labium differed between the sexes in mode and density of pilosity (e.g., in Triodontella Reitter, 1919). All species studied had prognathous mouthparts with symmetrical maxillae, labrum, epipharynx and labium. The paired mandibles are often slightly asymmetrical, with one molar lobe being convex and one concave. Across all species of Sericini examined, the labium is strongly sclerotized with two ligular lobes, which are either distinctly separated by a visible suture or are fused medially. Additionally, the ligular lobe was either fused with the prementum or separated from it by a suture. All species have a three-jointed labial palp (Fig. 1A, B). The labrum forms the dorsal pre-oral region and is positioned on the anterior and ventral surface of the clypeus (Nel & Scholtz 1990). The labrum of all the species is sclerotized anteriorly with a membranous and densely setose epipharynx posteriorly, which is often not completely symmetrical. The paired maxillae are situated between the mandibles and the labrum, and occupy the lateral margin of ventral surface of the preoral cavity (Fig. 1A). As in other Scarabaeidae, the maxilla consists of

3.2.1. Labium 1. Labium, ligular lobes: (0) distinctly separated (by a visible suture) (Fig. 1A); (1) entirely fused medially (Fig. 1B) (ci ¼ 0.11; ri ¼ 0.42). 2. Labium, ligular lobe and prementum: (0) separated by a suture (Fig. 1A); (1) fused (Fig. 1C) (ci ¼ 0.1; ri ¼ 0.47). 3. Labium, broadest part: (0) at apex (level of ligular lobe) (Fig. 1C); (1) between prementum and mentum (preapical) (Fig. 1B); (2) median (at the middle of labium) (Fig. 1A) (ci ¼ 0.12; ri ¼ 0.46). 4. Labium, palpiger: (0) fused with prementum (Fig. 1C); (1) fused with ligular lobe (Fig. 1D); (2) not fused (completely separated by a suture) (Fig. 1B) (ci ¼ 0.33; ri ¼ 0.55).

3.2.2. Maxilla 5. Maxilla, galea, relationship between galeal teeth in ventral row: (0) teeth all well separated from each other (Fig. 1F); (1) teeth all fused with each other (Suppl. Fig. 47K) (ci ¼ 0.5; ri ¼ 0). 6. Maxilla; galea, separation of galeal teeth from galeal body: (0) all teeth solidly fused with body of galea (Fig. 1F); (1) with a median tooth that is separated by a membrane from base of galea (Fig. 1E) (uninformative). 7. Maxilla, galea, distribution of dorsal galeal teeth along galeal mesal surface: (0) teeth of dorsal row distributed over entire galea length (Fig. 1F); (1) teeth of dorsal row with a large gap

58

J. Frings et al. / Zoologischer Anzeiger 284 (2020) 53e65

Table 2 Character matrix.

Sparrmannia sp. Diphucephala sp. Heteronyx sp. Cyrtocamenta sp. Ablaberoides abyssinicus 1 Ablaberoides abyssinicus 2 Ablaberoides moestus Ablaberoides somalicola Ablaberoides sp. Co1 male Ablaberoides sp. Co1 female Allokotarsa sp. 1 female Allokotarsa sp. 1 male Allokotarsa sp. 2 female Allokotarsa sp. 2 male Alogistotarsa sp. Spit1 female Alogistotarsa sp. Spit1 male Alogistotarsa straminea female Alogistotarsa straminea male Amaladera euphorbiae Amiserica flavolucida Amiserica krausei Amiserica rufidula Anomalophylla tristicula Anomioserica flavipes Archaeomalopia abbreviata Arraphytarsa sp. female Arraphytarsa sp. male Astaena sp. Bilga sp. Calloserica langtangica Camentoserica livida Charioserica striata Chrysoserica auricoma Comaserica bergrothi Cycloserica excisipes Deroserica pulchra Dissotoxus isignicornis Dolerotarsa emendatrix Emphania metallica Eriphoserica camentoides Eumaladera subrugata Euronycha rhodisiana Euserica villareali Gastromaladera major Gastroserica carolusi Gastroserica huaphanensis Gastroserica marginalis Gastroserica sp. female Glaphyserica humeralis Gryphonycha puberula Gynaecoserica cymosa Gynaecoserica minutula Hellaserica elongata Hetamius demaisoni Heteroserica hovana Hoplomaladera shibtai Hyboserica alexandriana Hymenochelus distinctus Hymenoplia castilliana Hyposerica cruciata Lasioserica brevipilosa Lasioserica modikholae Lasioserica nobilis Lepidoserica maculifera Lepiserica zoutpaniana Leucoserica arenicola Leuroserica lateralis Maladera clypeata Maladera drescheri Maladera fuscescens Maladera holosericea Maladera hongkongica Maladera marginella

1

1111111112

2222222223

3333333334

4444444445

55

1234567890

1234567890

1234567890

1234567890

1234567890

12

1121000200 0010010011 1122010011 1110000301 1020000211 1000000211 1010000211 1000000211 1020000111 1020000111 1000000111 1000000111 1000000101 1000000101 1000000111 1000000111 1010000111 1010000111 0000000211 1000000211 1020000211 1000000201 1100000211 1000000211 0000000201 1000000111 1000000111 1001000311 1100000211 1000000211 1000000111 0020000211 1000000211 0000000211 1000000211 1000000211 0000000211 1000000211 0000000211 1000000111 1000000211 1102000311 1100000211 1000000211 1000000211 1000000211 1000000211 1000000211 1010000011 1000000211 1000000211 1000000211 1011000211 1122000311 1010000111 1000000211 1100000211 1120001211 1100001211 0020000211 1000000211 1000000211 1000000211 1000000211 1000000211 1000000111 1000000211 1000000211 1000000211 1000000211 1000000211 1000000211 0000000211

0-1010-100 0022013011 1121013101 0000011010 0000014000 0000014000 0000014000 0001015000 0020014000 0020014000 0000014000 0000014000 0001014000 0001014000 0010014000 0010014000 0010014000 0010014000 0010010001 0010016001 0020010000 0101016000 0010016001 0010013000 0110010000 0000014000 0000014000 0010013002 0100015000 0001015001 0110013001 0010010000 0101015000 0111010000 0020010001 0010013001 0110010000 0001013000 0111015000 1120013001 0000016001 1020012000 0010010001 ?0?0010001 0011016001 0021016001 0011016001 0011016001 0111010000 0011015000 0010015000 0010015000 0110013011 0020012000 0110013000 0001016001 0010010001 0020012000 0120012000 0110015000 0110015001 0101015001 0111015001 0101010001 0010015001 0110010000 0010016000 0001016001 0010016001 0010016001 0010010001 0010016001 0011016001

0000001120 1120001120 1020?????? 1001010110 0001111110 0001111110 0001111010 0001111110 0001111110 0001111110 0001111110 0001111110 0001111110 0001111110 0001111110 0001111110 0001111110 0001111110 0001110110 0101110000 0101110110 0101110111 0001110110 0001010010 0001110110 1001111110 1001111110 0001010010 0001110010 0101010021 0101110110 0001110010 0101010011 0101010110 0001100120 0011100110 0101010010 1001111010 0101110110 0101110120 0001110011 1021010110 0001010110 0101110111 0001010110 0001010110 0001010111 0001110111 0111010120 0001110010 0101110000 0101110011 1101010010 1021010011 0101100110 0101110110 0101110010 1021?????? 1001110020 0101110010 0101010111 0101110111 0101110111 0101110010 0001110010 0011110111 0001110110 0001100111 0001110011 0001110011 0101000110 0001110111 0011100111

11000e101 1111122213 ??01111102 1101102000 1011130021 1011130021 1111130220 1111130120 1111130020 1111130020 1121130221 1121130221 1121130221 1121130221 1121130021 1121130021 1021131021 1021131021 0011121020 0111120120 0111110020 0111120220 0111120020 0011111020 0111120020 1121130021 1121130021 2111111110 2121110222 0111111113 0011120020 1111111010 0111120020 1111111010 0111120120 0111120220 1111120020 1111130110 1111121013 0011121020 0111120020 1111121010 0011120020 01111?0120 0111120113 1111120113 0011120113 1111120113 0111121120 0011120020 0111120120 0011121020 0011110010 1111121010 1111121010 0111120120 1111111013 ???1111010 1111110000 0111121020 0011120121 0111120120 1111120113 0111120123 0011120020 0111120020 0011120020 0011120020 0011120020 0011110010 0111121020 0011120020 0111120010

013-011111021010000 003-00110003-001112001110100 2101110100 1111110100 2011211100 2101110100 2101110100 1101110100 1101110100 1101110100 1101110100 2101110100 2101110100 2101110100 2101110100 1011210100 0011210100 1010210101 1111210100 2021210101 1011210100 1010020100 1101110100 1101110100 1021000100 1121120100 0021200101 2111211101 1010000100 1121210101 1121010100 1010210101 1121210101 0121010101 1010111100 1021010101 2011210100 1021210100 1111101100 0101210100 0021210100 0121210100 0121210101 0121010101 0021210101 0020010001 1001210100 0011210100 1011210100 0010000001 0011101100 2111210100 1121210100 0021010100 10???????? 0020000000 1011000100 0011210100 0121010101 0121010000 1121010100 1021210100 2001010101 0011210100 1021210101 1021210100 1021210100 1020010101 1021010100 1021210101

0 00 0 0 ?2 12 12 12 12 12 11 11 11 11 12 11 12 11 11 11 10 11 11 10 11 11 11 11 11 12 11 10 11 02 11 10 01 11 01 12 10 00 11 01 12 12 12 12 02 12 11 11 02 10 12 12 12 ?? 01 00 11 02 02 11 11 12 11 12 11 11 11 1? 12

J. Frings et al. / Zoologischer Anzeiger 284 (2020) 53e65

59

Table 2 (continued )

Maladera punctatissima Maladera secreta Maladera setosa Maladera simlana Maladera straba Maladera sp. Maladera sp. (close hongkongica) Maladera thomsoni Meriserica oberthuri Microserica interrogator Microserica quadrimaculata Microserica sp. Microserica varians Microsericaria quadripunctata Microtrochalus plagiger Nedymoserica flavida Neomaladera barbara Neoserica allolaotica Neoserica calva Neoserica martinui Neoserica uniformis Nepaloserica rufescens Nesoserica ursina Neuroserica mashoana Nipponoserica koltzei Omalopia erythroptera Omalopia nigromarginata Omalopia ruricola ruricola Omalopia spirea Oxyserica pygidialis Pachyserica olafi Paraserica grisea Paratriodonta romana Periserica picta Philoserica vittata Phylloserica sp. Pleophylla fasciatipennis Plotopuserica darwiniana Pseudosericania makiharai Selaserica nitida Serica brunnea Serica fusa Serica heydeni Serica intermixta Serica kingdoni Serica nigroguttata Serica thibetana Sericania fuscolineata Stilbolemma sericea Straliga croceicollis Symmela pallipes Synacta corrugata Taiwanoserica anmashanica Tetraserica brahmaputrae Tetraserica sp. Trichomaladera yui Triodontella aquilla female Triodontella aquilla male Trochaloserica festiva Trochalus byrrhinus Trochalus ferregineus Xenoserica brachyptera

1

1111111112

2222222223

3333333334

4444444445

55

1234567890

1234567890

1234567890

1234567890

1234567890

12

1000000211 1000000211 1000000111 1000000211 1000000211 1000000211 1000000211 1000000211 1000000211 1000000211 1000000211 1000000211 1000000211 1000000211 ?000000211 1000000211 1000000211 1000000211 1000000211 1000000211 1000000211 1000000211 1000000211 1000000201 1000000211 0021000211 0011000211 0021000211 0011000211 1000000211 1000000211 1000000211 1110000311 1000000211 0000000101 1100001111 1100000211 0000102211 1100000211 1000000201 1000000201 1000000211 1000000211 1000000211 1000000201 1000000211 1000000201 1000000211 1000000211 1020000211 1001000311 0020000101 1000000211 1000000211 1000000211 1100000211 1110000311 1110000311 1010000111 1010000211 1000000211 1000000211

0010015001 0001016001 0011015001 0011016001 0011016001 0010015001 0000016001 0010016001 0001013000 0010016001 0110015000 0010010000 0000016001 0010013001 0000014000 0010016000 0010010001 0101010001 0010010000 0010016001 0011016001 0101010001 0011016001 0020016000 0001016001 0110013010 0120013011 0110013010 0120010010 0010015001 0110016001 0010016000 0120012000 0011010000 0010016000 0111013000 0011013011 0001013001 0010016000 0001010000 0001016001 0010016001 0111016000 0000016001 0101016001 0011016001 0101016001 0010010001 0010016001 0011010000 0012013001 0110015001 0011010001 0010015000 0010015000 0001012001 0020012000 0110012000 0000014000 0010015000 0000015000 0011015001

0101110111 0001110011 0101110111 0001100111 0101110111 0001010110 0001010111 0001110010 0001100021 0001110111 0001110011 0001010111 0001110111 0011110111 1001111110 0001110110 0001110110 0101010110 0001110111 0001110110 0001110111 0101010111 0001010110 0001110110 0001010121 1101010110 1101010110 1101010110 1121100120 0001110011 0101100110 0001010110 1121010020 0101110010 0001110110 0001110010 1111010110 0101110021 0001010110 0101110010 0101010110 0101010000 01010101?1 0001010110 0101010110 0001110110 0101010110 0101010120 0001010110 0101110110 0001110010 0001110010 0001010111 0001010010 0001010010 0001010120 1001110110 1001110110 0001111110 0001110011 0001110011 0001110110

0011120120 0111120020 0111120020 0011121020 01111?0120 0011121020 0011120120 0011120020 0111120120 0111120020 1121121020 0111120020 0011121020 0111120220 1111130020 0011120120 0111110010 0111120120 0111120210 0011120020 0111120020 0011120020 0111120020 1111120020 0111120020 0111121020 0111111010 0111121010 0011110010 0111120020 0111120020 0011120020 1111120000 0011110020 0011120020 1111120110 0011111210 0111111010 0011120020 1111121113 0111120020 0111120020 0011120020 0011110020 0011120020 1111110020 0111120020 0111120020 0111120010 1011121010 0111121010 1011121011 0011120220 1111120020 1111121120 0011130123 1111121010 1111121010 1121130020 1121120121 1121120121 0011120010

1021210101 1021210100 2010210100 1021210100 1021210100 1021210100 1021210101 1021210100 2021210101 1021010101 2121210100 1011210100 1011210100 1111010100 1101110100 0021010100 1011210100 1021111100 1111200100 1121210100 0021010100 1121210100 0111210100 0001211100 1111210100 0020210000 0010211000 0010210100 0010211100 1010201101 0021210100 0021010100 0020000010 0021210100 1011210100 1020001101 2010020000 013-011110011210100 1021010101 0111210100 1021210101 1011210100 1011210100 0010200100 1121210100 0021210100 0011210100 1011210100 1011001000 1010200100 1011010100 0011210100 1021210101 1021210101 0011210101 0011101100 0011101100 1001110100 1121010101 1121010101 1011210100

11 11 11 12 11 12 11 10 12 10 11 11 11 11 12 00 11 12 11 11 11 12 11 10 11 00 01 01 10 10 12 10 00 11 12 02 00 0 12 02 12 12 12 11 11 10 12 12 11 11 01 10 11 12 11 12 10 10 12 01 01 12

between apical and basal teeth (Fig. 1G); (2) teeth of dorsal row situated only in basal part (ci ¼ 0.5; ri ¼ 0). 8. Maxilla, number of teeth of galea: (0) five (Fig. 1E); (1) six (Fig. 1H); (2) seven (Fig. 1G); (3) eight (Fig. 1K); (4) without any teeth. [We refrained to separate this character state into the ventral and dorsal portion, as assignment of basal and apical tooth is often ambiguous.] (ci ¼ 0.23; ri ¼ 0.64).

9. Maxillary palpus: (0) as long as the basistipes (Fig. 1H); (1) distinctly shorter than the basistipes (Fig. 1E) (ci ¼ 0.08; ri ¼ 0.26). 10. Distal sensory area of distal maxillary palpomere: (0) absent (Fig. 1I); (1) present (Fig. 1E) (uninformative). 11. Distal segment of maxillary palpus: (0) narrowed towards apex (Fig. 1I); (1) widened at apex (Fig. 1J) (ci ¼ 0.33; ri ¼ 0).

60

J. Frings et al. / Zoologischer Anzeiger 284 (2020) 53e65

12. Distal sensory area of distal palpomere: (0) small (extension less than half maximum width of distal palpomere) (Fig. 1E); (1) large (its extension more than half of maximum width of distal palpomere) (Fig. 1J) (ci ¼ 0.06; ri ¼ 0.58). 13. Distal maxillary palpomere; ratio, length/width: (0) more than 3 times as long as wide (Fig. 1H); (1) more than twice but less than three times as long as wide (Fig. 1I); (2) less or equal than twice as long as wide (Fig. 1G) (ci ¼ 0.08; ri ¼ 0.57). 14. Penultimate maxillary palpomere; Ratio, length/width: (0) as long as wide (Fig. 1I); (1) distinctly longer than wide (Fig. 1L); (2) wider than long (Fig. 1E) (ci ¼ 0.12; ri ¼ 0.68). 15. Maxillary palpus: (0) without dorsal longitudinal groove (Fig. 1L); (1) with deep dorsal longitudinal groove (Fig. 1I) (uninformative). 16. Maxilla, presence of dorsal process of mediostipes: (0) absent (Fig. 1I); (1) present (Fig. 1L) (uninformative). 17. Maxilla, shape of dorsal process of mediostipes: (0) narrow and nearly evenly narrowed towards apex (Fig. 1M); (1) extremely (axe-like) widened anteriorly and posteriorly (Fig. 1O); (2) condylus-like enlarged at apex (Fig. 1N); (3) rather broad, evenly narrowed toward apex (Fig. 1P); (4) rather broad but abruptly and convexly narrowed (distal portion) towards apex (Fig. 1R); (5) moderately broad, evenly narrowed towards apex (Fig. 1Q); (6) moderately broad, internal margin abruptly widened well before apex (Fig. 1S) (ci ¼ 0.18; ri ¼ 0.70). 18. Maxilla: mediostipes: (0) not extended distally, ending well before galea (Fig. 1Q); (1) extended distally, expanding over level of galea (Fig. 1T) (ci ¼ 1; ri ¼ 1). 19. Lacinia length relative to length of galea: (0) as long, slightly longer or slightly shorter than length of galea (Fig. 1K); (1) at maximum half as long as length of galea (Fig. 1L) (ci ¼ 0.5; ri ¼ 0.83). 20. Lacinia length relative to its width: (0) at least 3 times longer than its width (Fig. 1R); (1) 2 times longer than its width (Fig. 1T); (2) subequal to its width (Fig. 1P) (ci ¼ 0.11; ri ¼ 0.76). 21. Lacinia, apically: (0) broadened (at apical quarter wider than at middle) (Fig. 1R,S); (1) narrowed (at apical quarter as narrow or narrower than at middle) (Fig. 1O, T) (ci ¼ 0.16; ri ¼ 0.72). 22. Lacinia, basally: (0) distinctly fused with mediostipes (Fig. 1R); (1) not distinctly fused with mediostipes (Fig. 1N) (ci ¼ 0.07; ri ¼ 0.73). 23. Apex of lacinia: (0) convexly rounded (Fig. 1S); (1) nearly truncate (Fig. 1U); (2) sharp (Fig. 1T) (ci ¼ 0.22; ri ¼ 0.3).

3.2.3. Labrum and epipharynx 24. Labrum dorsally: (0) separated from clypeus (Fig. 1V); (1) at least in part fused with clypeus (Fig. 1W) (ci ¼ 1; ri ¼ 1). 25. Distal and lateral edge of epipharynx: (0) distinctly fused with the labrum (Fig. 1X); (1) not distinctly fused with the labrum (Fig. 1W) (ci ¼ 0.04; ri ¼ 0.48). 26. Epipharynx (ventral view), distal margin on each side: (0) tooth-like protruding (Fig. 1V); (1) rounded (Fig. 1W) (ci ¼ 0.11; ri ¼ 0.2). 27. Distance between apical lateral lobes of epipharynx (in relation to total width of labroclypeus): (0) narrow (less than half of width of labroclypeus) (Fig. 2A); (1) wide (more than half of width of labroclypeus) (Fig. 1X) (ci ¼ 0.5; ri ¼ 0.94). 28. Median portion of labrum: (0) not sinuated (at the same level in comparison to the most distal portion of labrum) (Fig. 2A); (1) sinuated medially (displaced basally at middle in

29.

30. 31.

32.

comparison to the most distal portion of labrum) (Fig. 1X) (ci ¼ 0.05; ri ¼ 0.58). Median sinuation of epipharynx: (0) absent (Fig. 2B); (1) very shallow (about a quarter as deep as sinuation wide) (Fig. 1W); (2) deep (more than a third as deep as sinuation width) (Fig. 1V) (ci ¼ 0.18; ri ¼ 0.35). Labrum, bristles of the chaetopariae: (0) straight (Fig. 1W); (1) curved (Fig. 2C) (ci ¼ 0.05; ri ¼ 0.51). Bristles of chaetopariae: (0) in a single row (Fig. 1W); (1) unordered (Fig. 1V); (2) in two rows (Fig. 2D) (ci ¼ 0.14; ri ¼ 0.74). Number of setae of chaetopariae in the sclerotised portion of epipharynx: (0) 4 or less (Fig. 2E); (1) 5 or more (Fig. 2B) (ci ¼ 0.04; ri ¼ 0.5).

3.2.4. Mandible 33. Mandible (dorsal view); ratio of mandible length versus [longitudinal] extension of molar lobe: (0) distinctly less than 1/3 (Fig. 2F); (1) ca 2/3 (Fig. 2G); (2) 1 (Fig. 2H) (ci ¼ 0.5; ri ¼ 0.87). 34. Mandible; pectineus medialis: (0) strongly sclerotised (Fig. 2I); (1) widely membranous (Fig. 2J) (uninformative). 35. Mandible; sutura interna of callus lateralis: (0) absent (Fig. 2I); (1) present (Fig. 2J) (uninformative). 36. Mandible (ventral view), sutura interna (S-I) of callus lateralis: (0) not curved (Fig. 2N); (1) slightly curved (Fig. 2K); (2) distinctly curved (Fig. 2L); (3) subangulate (Fig. 2M) (ci ¼ 0.15; ri ¼ 0.56). 37. Mandible; widest interior extension of disc of callus lateralis (defined interiorly by the sutura interna): (0) basally (Fig. 2O); (1) mesal (Fig. 2K); (2) distal (Fig. 2N) (ci ¼ 0.11; ri ¼ 0.57). 38. Mandible, sutura externa of callus lateralis (in its central portion of two third of its length): (0) straight (Fig. 2N); (1) convexly curved (Fig. 2K); (2) concavely sinuated (Fig. 2L) (ci ¼ 0.09; ri ¼ 0.52). 39. Mandible (ventral view): (0) longer than wide (Fig. 2N); (1) as long as wide (Fig. 2O); (2) shorter than wide (Fig. 2M) (ci ¼ 0.12; ri ¼ 0.63). 40. Mandible; apicalis (i.e., apical portion) at apex (Fig. 2G: a): (0) blunt, moderately rounded (Fig. 2K); (1) nearly rectangular (Fig. 2M); (2) sharply angulate (Fig. 2H); (3) strongly rounded (Fig. 2P) (ci ¼ 0.18; ri ¼ 0.51). 41. Mandible; between distal portion of apicalis and distal tooth of apicalis: (0) straight or convex, not concavely sinuate (Figs. 2N and 3P); (1) moderately sinuate (Fig. 2O); (2) deeply sinuate (Fig. 2Q) (ci ¼ 0.08; ri ¼ 0.63). 42. Mandible; distal tooth of apicalis (Fig. 2G: dta): (0) less than half as long as width of base of mandible (Fig. 2F); (1) at least half as long as width of base of mandible (Fig. 2H) (ci ¼ 0.05; ri ¼ 0.59). 43. Mandible (molar lobe); number of teeth rows: (0) 4 or less rows (Fig. 2R); (1) 5e8 rows (Fig. 2T); (2) 9 or more rows (Fig. 2U); (3) without teeth (Fig. 2S) (ci ¼ 0.13; ri ¼ 0.72). 44. Mandible; most distal row of teeth of molar lobe: (0) not enlarged (Fig. 2U); (1) at least twice as high as other rows of teeth (Fig. 2V) (ci ¼ 0.09; ri ¼ 0.47). 45. Mandible; basal carina of distal lobe: (0) basally (Fig. 2U); (1) completely displaced medially (Fig. 2R); (2) only on ventral portion displaced medially (Fig. 2W) (ci ¼ 0.12; ri ¼ 0.75). 46. Mandible, carina basalis: (0) weakly curved, nearly straight (Fig. 2U); (1) moderately curved (Fig. 2V); (2) strongly curved (Fig. 2W) (ci ¼ 0.16; ri ¼ 0.5).

J. Frings et al. / Zoologischer Anzeiger 284 (2020) 53e65

61

Fig. 3. Majority rule consensus tree (divided in two parts) generated with Winclada showing unsupported nodes collapsed and using proportional branch lengths. The numbers above the branches indicate the frequency of the node among all maximum parsimonious trees.

47. Mandible; basidorsal portion of lobus molaris: (0) with teeth (Fig. 2U); (1) without teeth (Fig. 2W) (ci ¼ 0.09; ri ¼ 0.41). 48. Mandible; basiventral portion of lobus molaris: (0) with teeth (Fig. 2U); (1) without teeth (Fig. 2V) (ci ¼ 0.16; ri ¼ 0.37). 49. Mandibular brush: (0) well developed (Fig. 2W); (1) small (Fig. 2S) (ci ¼ 0.25; ri ¼ 0). 50. Mandible; tooth rows: (0) straight (Fig. 2U); (1) curved (Fig. 2X) (ci ¼ 0.05; ri ¼ 0.48). 51. Mandible; tooth rows on central portion of medial lobe: (0) complete, covering central portion with its entire length (Fig. 2U); (1) short, covering only small part of central portion (Fig. 2V) (ci ¼ 0.11; ri ¼ 0.61).

52. Mandible, sutura externa of callus lateralis ending: (0) well before lateral margin of mandible (Fig. 2L); (1) laterally nearly (at least in apical part) close to the lateral margin (Fig. 2M); (2) at the same level of beyond the lateral margin, which is not visible in ventral view (Fig. 2P) (ci ¼ 0.05; ri ¼ 0.52). 3.3. Phylogenetic analysis Out of 52 adult mouthparts characters, 6 were uninformative, while 46 were parsimony-informative. The degree of homoplasy among characters was high, the mean of single consistency index of each character was only 0.16. Our dataset had very few missing data

62

J. Frings et al. / Zoologischer Anzeiger 284 (2020) 53e65

points: in Heteronyx sp. (8 characters missing for the epipharynx), Hymenochelus distinctus (Uhagon, 1876) (9 characters for the epipharynx and 10 characters for the mandible) and in Maladera straba (Brenske, 1898) (one character for the mandible). Analysis using the parsimony ratchet yielded 3 equally parsimonious trees of 617 steps (CI ¼ 0.13, RI ¼ 0.6). Repeating the ratchet 100 times neither improved tree length nor decreased the number of equally parsimonious trees found. The majority rule consensus tree, which represents all monophyletic nodes that occurred in more than 50% of the 3 equally parsimonious trees, is shown in Fig. 3. The strict consensus tree, including bootstrap values, is presented in Fig. 4. All unambiguous character changes were mapped along each branch of this tree. The strict consensus topology was to a strong degree polytomous. Bootstrap values were generally weak, only a few nodes had values above 50 (Fig. 4). Only a few of the clades of the MRT were also consistent in the strict consensus tree: one clade comprising five Asian species and three African species was present in both trees (Figs. 3 and 4; node A), the clade containing the Trochalina (node D), as well the basal branching nodes up to the node of subtribe Sericina. Ablaberini was indicated as sister to Sericini, both tribes were monophyletic. Neither of the currently recognized Sericine subtribes, Trochalina and Sericina, were recovered as monophyletic in either of the consensus trees (Figs. 3 and 4). Within subtribe Sericina were recovered also two clades of ancient lineages (non-Sericina; nodes B, C) and also the Trochalina resulting here paraphyletic. Nevertheless, the genera belonging to the subtribe Trochalina were grouped at the tip of the tree; however, within a clade containing nine other Sericina (node D). The South America lineage (Astaena Erichson, 1841 þ Symmela Erichson, 1835) nested within the anicient old World lineages such as Omaloplia, Triodontella, Hyposerica Brenske, 1897 etc. Some of the less extensively sampled genera appeared to be monophyletic (Figs. 3 and 4) (e.g., Tetraserica Ahrens, 2004, Gastroserica Brenske, 1897, and Allokotarsa), while other well defined groups such as Serica (subgenus Serica McLeay, 1819) (Ahrens 2007c), which was included here with four species, were polyphyletic. Lasioserica Brenske, 1896 appeared to be paraphyletic as well, being found in two separate clades. Likewise, Gynaecoserica Brenske, 1896, represented here by two species, was recovered also as paraphyletic. The Triodontella lineage (Eberle et al. 2017) containing species of Euronycha Peringuey, 1904, Hetamius Fairmaire, 1893, Triodontella, Hymenochelus Reitter, 1890, Paratriodonta Baraus, 1964 examined during this study appears polyphyletic. The genus Omaloplia represented with four species was monophyletic, with Hellaserica Baraud & Nicolas, 1966 þ Pleophylla Erichson, 1847 nested as sister to Omaloplia. 4. Discussion Traditional definitions of most genera in Sericini are principally based on works of Reitter (1896, 1902) and Brenske (1897, 1899), as well as subsequent authors (Moser 1915, 1916 1917, 1918 1920, 1922 1924; Frey 1960, 1965 1968, 1969 1970, 1973 1974; Nomura 1973, 1974). One major diagnostic character these authors often used was the specific configuration of antennomeres in the antennal club. Later studies (e.g., Ahrens 2004; Fabrizi & Ahrens 2014; Ahrens & Fabrizi 2016) continued to use number of antennomeres as a major diagnostic character; however, significant evolutionary plasticity has been recognized for this character trait (Ahrens & Vogler 2008). In the present study, we assessed comparative criteria for the mouthparts of Sericini and used them to reconstruct a phylogenetic tree. Tree resolution and branch support was suboptimal. The basal

branches of the Sericini are poorly resolved, and terminal branches also show only low support. Given the low bootstrap support, we refrained of infering other measures of branch support at this point. The topology of the consensus trees (Figs. 3 and 4) revealed pectinate or polytomous results. A consistency index (CI) of 0.13 and retention index (RI) of 0.6 (Fig. 4) is rather low, but not that unusual for a small matrix with only 52 character states and 134 terminals. Our trees did not confirm the monophyly of the two major subtribes Sericina (Figs. 3 and 4) and Trochalina, both found in several studies to be monophyletic (Ahrens & Vogler 2008; Liu et al. 2015; Eberle et al. 2017). Therefore, for a complete sampling of Sericini, many more characters must be used in order to reconstruct a robust phylogenetic tree based on morphology, i.e., a full set of morphological data and not just specific data for individual structures or systems. Characters that are more informative must be found, and discovering these will be the challenge for all future studies. However, as indicated by the present study, options appear limited for extension of the current mouthpart data matrix for many more characters. The alternative solution, to map morphology onto a molecular phyleogentic tree, is also no option, since for many of the genera examined here based on morphology no molecular data are so far available. During evolution, mouthparts would be expected to undergo modifications and/or adaptations due to various selective pressures such as different feeding behaviours and niche specialization. For instance, simply observe the various lengths and designs of proboscises that have developed in nectar feeding insects (Krenn et al. 2005). Likewise, modified mouthparts are apparent in several lineages of scarab beetles, ranging primitively mandibulate to structures incapable of chewing solid food and being modified to consume liquid (Nel & De Villiers 1988). Adult phytophagous Sericini are thought to have diversified with the rise of angiosperms in the Cretaceous (around 108 Mya) (Wang et al. 2013; Ahrens et al. 2014; Eberle et al. 2017). The rapid radiation of Sericini (Eberle et al. 2017) combined with a uniform life history of plant polyphagy, may explain the relatively uniform shape and lack of specialization in the mouthparts. Even flower-feeding species (e.g., Oxyserica Brenske, 1899 and Microserica Brenske, 1894) lack special modifications. The teeth on the molar lobes of H. castilliana (see Supplement Figure 28M), however, look somewhat different compared to other Sericini. They are rather numerous and fine; similar structures occur in groups that are adapted to eating pollen. However, given the rather immense age of the lineage of Sericini (see above), the general morphology in mouthparts of Sericini, even between pollen feeder and non pollen feeder, has to be evaluated as rather uniform and conservative. Mouth parts are much more derived and divergent form the general pleurostict groundplan in many even younger but specialized lineages of pollen feeders such as Hoplini, Valgini, Phyllotocini, Cetoniini etc (e.g., Ahrens 2006c; Karolyi et al. 2016). This could be an indicator that pollen feeding in Sericini, at least in some groups, is either rather young or that floricolous taxa feed in large extent on floral petals and not only exclusively on pollen. Despite the obvious limitations of the current mouthpart study for resolving the phylogeny of Sericini genera, it should be viewed as a primer for further study of other morphological structures, including mouthparts, of Sericini. Future progress in detailed studies and better understanding of various traits will be aided by using newer methods like micro-CT scanning, three-dimensional reconstructions and/or geometric morphometric methods (e.g., Bai et al. 2015). The results elaborated in this paper expand previous knowledge (Ahrens 2006c) of Sercini mouthparts considerably and represent a significant step towards a concerted analysis of the tribe. In the future, a much wider array of morphological traits

J. Frings et al. / Zoologischer Anzeiger 284 (2020) 53e65

63

Fig. 4. Strict consensus tree (divided in two parts) showing character changes and apomorphies mapped by state. Solid squares: non-homoplasious character states; open squares: homoplasious character states. Bootstrap values above 50 are shown below branches.

should be used, to increase clarity in the phylogeny and classification of Sericini. Declarations of interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements um We are grateful to Y. Cambefort and O. Montreuil (Muse national d’Histoire naturelle, Paris), M. Barclay and M. D. Kerley (Natural History Museum London) as well as, J. Frisch and M. Uhlig (Museum für Naturkunde, Berlin) for allowing access to the scarabaeid collections of their respective institutions and the loan of material for morphological study and dissection. Support for this

64

J. Frings et al. / Zoologischer Anzeiger 284 (2020) 53e65

project was provided by DFG grants GRK 503/2 and AH175/3 to D.A. We thank K. Klass (Senckenberg Museum Dresden) for his helpful comments on an earlier version of the manuscript. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi.org/10.1016/j.jcz.2019.11.008. References Ahrens, D., 2004. Monographie der Sericini des Himalaya (Coleoptera, Scarabaeidae). Dissertation.de - Verlag Im Internet GmbH, Berlin, p. 534. Ahrens, D., 2006a. Evolution of Asian “lowland” taxa in relation to the AlpineHimalayan tertiary orogenic belt - insight from a cladistic analysis of Maladera (Cycloserica) (Coleoptera: Scarabaeidae: Sericini). Zool. Anz. 244, 193e203. https://doi.org/10.1016/j.jcz.2005.10.002. Ahrens, D., 2006b. Phylogenetische Analyse und Revision der Arten der Gattung Pachyserica Brenske , 1897 ( Coleoptera , Scarabaeidae , Sericini ). Rev. Suisse Zool. 113, 487e557. Ahrens, D., 2006c. The phylogeny of Sericini and their position within the Scarabaeidae based on morphological characters (Coleoptera: Scarabaeidae). Syst. Ent. 31, 113e144. https://doi.org/10.1111/j.1365-3113.2005.00307.x. Ahrens, D., 2007a. Taxonomic changes and an updated catalogue of Palaearctic Sericini (Coleoptera: Scarabaeidae: Melolonthinae). Zootaxa 1504, 1e51. Ahrens, D., 2007b. Type species designations of Afrotropical chafer genera of Ablaberini and Sericini (Coleoptera: Scarabaeidae: Melolonthinae). Zootaxa 1496, 53e62. Ahrens, D., 2007c. Beetle evolution in the Asian highlands: insight from a phylogeny of the scarabaeid subgenus Serica (Coleoptera, Scarabaeidae). Syst. Entomol. 32, 450e476. Ahrens, D., Schwarzer, J., Vogler, A.P., 2014. The evolution of scarab beetles tracks the sequential rise of angiosperms and mammals. Proc. R. Soc. B 281, 20141470. Ahrens, D., Scott, M., Vogler, A.P., 2011. The phylogeny of monkey beetles based on mitochondrial and ribosomal RNA genes (Coleoptera: Scarabaeidae: Hopliini). Mol. Phylog. Evol. 60, 408e415. https://doi.org/10.1016/j.ympev.2011.04.011. Ahrens, D., Vogler, A.P., 2008. Towards the phylogeny of chafers (Sericini): analysis of alignment-variable sequences and the evolution of segment numbers in the antennal club. Mol. Phylog. Evol. 47, 783e798. https://doi.org/10.1016/ j.ympev.2008.02.010. Ahrens, D., Fabrizi, S., 2016. A monograph of the Sericini of India (Coleoptera: Scarabaeidae). Bonn Zool. Bull. 65, 1e355. Anton, E.A., Beutel, R.G.B., 2004. On the head morphology and systematic position of Helophorus (Coleoptera : Hydrophiloidea : Helophoridae ). Zool. Anz. 242, 313e346. https://doi.org/10.1078/0044-5231-00107. Anton, E.A., Beutel, R.G.B., 2012. The adult head morphology of Dascillus (L.) (Dascilloidea: Dascillidae) and Glaresis Erichson (Scarabaeoidea: Glaresidae) and its phylogenetic implications. Arthr. Syst. Phyl. 70, 3e42. Bai, M., Li, S., Yang, H., Tong, Y., Yang, X., 2015. Mandible evolution in the Scarabaeinae (Coleoptera: Scarabaeidae) and adaptations to corophagous habits. Fronti. Zool. 12, 30. https://doi.org/10.1186/s12983-015-0123-z. Ball, G.E., Acorn, J.H., Shpeley, D., 2011. Mandibles and labrum-epipharynx of tiger beetles: basic structure and evolution (Coleoptera, Carabidae, Cicindelitae). ZooKeys 147, 39e83. https://doi.org/10.3897/zookeys.147.2052. Betz, O., Thayer, M.K., Newton, A.F., 2003. Comparative morphology and evolutionary pathways of the mouthparts in spore-feeding Staphylinoidea ( Coleoptera ). Act. Zool. 84, 179e238. Beutel, R.G., 1994. Phylogenetic analysis of Hydrophiloidea based on characters of the head of adults and larvae ( Coleoptera : Staphyliniformia ). Kol. Rundsch. 64, 103e131. Blanke, A., Rühr, P., Mokso, R., Villanueva, P., Wilde, F., Stampanoni, M., Uesugi, K., Machida, R., Misof, B., 2015. Structural mouthpart interaction evolved already in the earliest lineages of insects. Proc. R. Soc. B 282, 20151033. https://doi.org/ 10.1098/rspb.2015.1033. Brenske, E., 1897. Die Serica - Arten der Erde. I. Berl. Ent. Ztschr. 42, 345e438. Brenske, E., 1899. Die Serica - Arten der Erde. III. Berl. Ent. Ztschr. 44, 161e272. Burmeister, H.C.C., 1855. Handbuch der Entomologie. Vierter Band. Besondere Entomologie. Fortsetzung. Zweite Abtheilung. Coleoptera Lamellicornia Phyllophaga chaenochela. Theod. Chr. Friedr. Enslin, Berlin, p. 569. Cabrero-Sanudo, F.J., 2007. The phylogeny of iberian Aphodiini species (Coleoptera, Scarabaeoidea, Scarabaeidae, Aphodiinae) based on morphology. Syst. Ent. 32, 156e175. Dalla Torre, K.W., 1912. In: Junk, W., Schenkling, S. (Eds.), Scarabaeidae: Melolonthinae I, vol. 45. Coleopterorum Catalogus, pp. 1e84. Dellacasa, G., Dellacasa, M., Mann, D.J., 2010. The morphology of labrum (epipharynx, ikrioma and aboral surface) of adult Aphodiini (Coleoptera: Scrabaeidae: Aphodiinae), and its implications for systematics. Ins. Mundi 132, 9e24. Eberle, J., Fabrizi, S., Lago, P., Ahrens, D., 2017. A historical biogeography of megadiverse Sericini e another story “out of Africa”? Cladistics 33, 183e197. Erichson, W.F., 1847. Naturgeschichte der Insecten Deutschlands. In: Coleoptera, vol. 3. Nicolaische Buchhandlung, pp. 481e640.

Fabrizi, S., Ahrens, D., 2014. A monograph of Sericini of Srilanka (Coleoptera: Scarabaeidae). Bonn Zool. Bull. (Suppl. 61), 1e124. Frey, G., 1960. Studien über afrikanische und indische Melolonthidae (Col.). Ent. Arb. Mus. Frey 11, 318e324. € stlichen Himalaya (Col. Melolonth.). Frey, G., 1965. Neue Sericinen aus dem Nordo Khumbu Himal. 2, 88e93. Frey, G., 1968. Neue Sericiden aus Afrika und Madagascar mit Bestimmungstabelle der Westafrikanischen Aulacoserica- Arten (Col., Melolonth.). Ent. Arb. Mus. Frey 18, 199e228. Frey, G., 1969. Unbekannte afrikanische Sericinae (Col. Scarab.). Ent. Arb. Mus. Frey 19, 73e78. Frey, G., 1970. Coleoptera aus Nordostafrika.Melolonthidae und Rutelidae. Not. Entomol. 50, 1e7. Frey, G., 1973. Synopsis der südamerikanischen Sericinen. (Col., Scar., Melolonth.). Ent. Arb. Mus. Frey 24, 315e366. Frey, G., 1974. Neue Melolonthiden von den Expeditionen des ungarischen Natio€di-Younga nalmuseums in Budapest, gesammelt von den Herren Dr. S. Endro und Dr. J. Szunyoghy, sowie eine neue mittelamerikanische Gattung der Sericinae. Ent. Arb. Mus. Frey 25, 109e120. Goloboff, P., 1999. NONA, version 2.0. Published by the author, Tucum an. Hansen, M., 1991. The Hydrophiloid beetles phylogeny, classification and a revision of the genera (Coleoptera, Hydrophiloidea). Biol. Skr. 40, 1e367. Hayes, W.P., 1992. The external morphology of lachnosterna crassissima Blanch (Scarabaeidae, Coleop.). Amer. Micr. Soc. 41, 1e28. Karolyi, F., Hansal, T., Krenn, H.W., Colville, J.F., 2016. Comparative morphology of the mouthparts of the megadiverse South African monkey beetles (Scarabaeidae: Hopliini): feeding adaptations and guild structure. PeerJ 4, e1597. https://doi.org/10.7717/peerj.1597. Karolyi, F., Szucsich, N.U., Colville, J.F., Krenn, H.W., 2012. Adaptations for nectarfeeding in the mouthparts of long-proboscid flies (Nemestrinidae: Prosoeca). Biol. J. Linn. Soc. 107, 414e424. https://doi.org/10.1111/j.1095-8312.2012.01945.x. Krenn, H.W., 2007. Evidence from mouthpart structure on interordinal relationships in endopterygota? Systematics 65, 7e14. Krenn, H.W., Plant, J.D., Szucsich, N.U., 2005. Mouthparts of flower-visiting insects. Arthropod Struct. Dev. 34, 1e40. https://doi.org/10.1016/j.asd.2004.10.002. Labandeira, C., 1997. Insect mouthparts: ascertaining the paleobiology of insect feeding strategies. Ann. Rev. Ecol. Syst. 28, 153e193. https://doi.org/10.1146/ annurev.ecolsys.28.1.153. Li, S., Bai, M., Wang, X.-L., Yang, X., 2013. Adaptive evolution and functional analysis of the mouthparts in predatory flower chafers (Coleoptera : Scarabaeidae : Cetoniinae : Cremastocheilini). Chin. J. Appl. Ent. 50, 974e980. https://doi.org/ 10.7679/j.issn.2095-1353. Liu, W.-G., Eberle, J., Bai, M., Yang, X., Ahrens, D., 2015. A phylogeny of Sericini with particular reference to Chinese species using mitochondrial and ribosomal DNA (Coleoptera: Scarabaeidae). Org. Div. Evol. 15, 343e350. https://doi.org/10.1007/ s13127-015-0204-z. Machatschke, J.W., 1959. Phylogenetische Untersuchungen über die Sericini (sensu Dalla Torre 1912) (Coleoptera: lamellicornia, Melolonthidae). Beitr. Ent. 9, 730e746. Mathur, P.N., Khattar, N., Mathur, V.D., 1958. Morphology of the head capsule and mouthparts of Heliocopris bucephalus fabre (Coleoptera, Polyphaga, Scarabaeoidea, Scarabaeidae, Coprinae). Proc. Ind. Acad. Sci. B 48, 137e153. Moser, J., 1915. Weitere neue Serica-Arten. Stett. ent. Ztg. 76, 144e202. Moser, J., 1916. Neue Sericiden vom Belgischen kongo. D. E. Z. 1916, 233e268. Moser, J., 1917. Neue afrikanische Melolonthiden. (Col.). D. E. Z. 1917, 183e256. Moser, J., 1918. Neue Melolonthiden aus der Sammlung des Deutschen Entomologischen Museums zu Berlin Dahlem. Stett. ent. Ztg. 79, 209e247. Moser, J., 1920. Beitrag zur Kenntnis der Melolonthiden. Stett. ent. Ztg. 81, 3e28. Moser, J., 1922. Neue Serica-Arten aus der orientalischen Region. Stett. ent. Ztg. 83, 101e112. Moser, J., 1924. Neue Melolonthiden und eine Cetonide vom Congo belge (Col.Lamell.). D. E. Z. 1924, 162e171. Nel, A., De Villiers, W.M., 1988. Mouthpart structure in adult scarab beetles (Coleoptera: Scarabaeidea). Entomol. Gen. 13, 95e114. Nel, A., Scholtz, C.H., 1990. Comparative morphology of the mouthparts of adult Scarabaeoidea (Coleoptera). Ent. Mem. 80, 1e84. ISBN 0-621-12866-X. Nixon, K.C., 1999. The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15, 407e414. https://doi.org/10.1111/j.1096-0031.1999.tb00277.x. Nixon, K.C., 2002. Winclada (BETA), version 1.00.08. Published by the author, Ithaca. ^ ho ^-Gakuho ^ 23, 119e152. Nomura, S., 1973. On the Sericini of Japan. I. To ^ ho ^-Gakuho ^ 24, 81e115. Nomura, S., 1974. On the Sericini of Taiwan. To € Ozgül-Siemund, A., Ahrens, D., 2015. Taxonomic utility of female copulation organs in Sericini chafers (Coleoptera, Scarabaeidae), with special reference ro asymmetry. Contr. Zool. 84, 167e178. Philips, K.T., Pretorius, E., Scholtz, C.H., 2004. A phylogenetic analysis of dung beetles (Scarabaeinae : Scarabaeidae): unrolling an evolutionary history. Inv. Syst. 18, 53e88. Reitter, E., 1896. Uebersicht der mir bekannten palaearktischen, mit der Coleopteren-Gattung Serica verwandten Gattungen und Arten. Wiener Ent. Ztg. 15, 180e188. €ischen Fauna Reitter, E., 1902. Bestimmungs-Tabelle der Melolonthidae aus der europa €ndern, enthaltend die Gruppen der Pachydemini, und den angrenzenden La Sericini and Melolonthini, vol. 1901. Verh. Naturf. Ver. Brünn XL, pp. 93e303. Sanmartín, I., Martín-Piera, F., 2003. First phylogenetic analysis of the subfamily Pachydeminae (Coleoptera, Scarabaeoidea, Melolonthidae): the Palearctic Pachydeminae. J. Zool. Syst. Evol. Res. 41, 2e46.

J. Frings et al. / Zoologischer Anzeiger 284 (2020) 53e65 Scholtz, C.H., 1990. Phylogenetic trends in the Scarabaeoidea (Coleoptera). J. Nat. Hist. 24, 1027e1066. https://doi.org/10.1080/00222939000770631. Strong, E.E., Lipscomb, D., 1999. Character coding and inapplicable data. Cladistics 15, 363e371. https://doi.org/10.1111/j.1096-0031.1999.tb00272.x. Wang, B., Zhang, H., Jarzembowski, E.A., 2013. Early Cretaceous angiosperms and beetle evolution. Front. Plant Sci. 4, 360. https://doi.org/10.3389/fpls.2013.00360.

65

Wilhelmi, A.P., Krenn, H.W., 2005. Elongated mouthparts of nectar-feeding Meloidae (Coleoptera). Zoomorphology 131, 325e337. https://doi.org/10.1007/ s00435-012-0162-3. Williams, I.W., 1938. Comparative morphology of the mouth parts of the order Coleoptera treated from the standpoint of phylogeny. N. Y. Ent. Soc. XLVI, 245e289.