insects Article Molecular Phylogeny, Diversity and Zoogeography of Net-Winged Beetles (Coleoptera: Lycidae) Michal Masek 1, Michal Motyka 1, Dominik Kusy 1, Matej Bocek 1 , Yun Li 1,2 and Ladislav Bocak 1,* 1 Laboratory of Molecular Systematics, Department of Zoology, Faculty of Science, Palacky University, 71146 Olomouc, Czech Republic; [email protected] (M.M.); [email protected] (M.M.); [email protected] (D.K.); [email protected] (M.B.); [email protected] (Y.L.) 2 State Key Laboratory of Biocontrol, College of Ecology and Evolution, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China * Correspondence: [email protected] Received: 7 August 2018; Accepted: 28 October 2018; Published: 1 November 2018 Abstract: We synthesize the evidence from molecular phylogenetics, extant distribution, and plate tectonics to present an insight in ancestral areas, dispersal routes and the effectiveness of geographic barriers for net-winged beetle tribes (Coleoptera: Lycidae). Samples from all zoogeographical realms were assembled and phylogenetic relationships for ~550 species and 25 tribes were inferred using nuclear rRNA and mtDNA markers. The analyses revealed well-supported clades at the rank of tribes as they have been defined using morphology, but a low support for relationships among them. Most tribes started their diversification in Southeast and East Asia or are endemic to this region. Slipinskiini and Dexorini are Afrotropical endemics and Calopterini, Eurrhacini, Thonalmini, and Leptolycini remained isolated in South America and the Caribbean after their separation from northern continents. Lycini, Calochromini, and Erotini support relationships between the Nearctic and eastern Palearctic faunas; Calochromini colonized the Afrotropical realm from East Asia and Metriorrhynchini Afrotropical and Oriental realms from the drifting Indian subcontinent. Most tribes occur in the Oriental and Sino-Japanese realms, the highest alpha-taxonomic diversity was identified in Malesian tropical rainforests. The turn-over at zoogeographical boundaries is discussed when only short distance over-sea colonization events were inferred. The lycid phylogeny shows that poor dispersers can be used for reconstruction of dispersal and vicariance history over a long time-span, but the current data are insufficient for reconstruction of the early phase of their diversification. Keywords: Coleoptera; Elateroidea; Lycidae; molecular phylogeny; zoogeography; zoogeographic realms; zoogeographic boundaries; diversity 1. Introduction The dispersal propensity and ecological adaptability substantially affect the extant distribution of animals and therefore, the zoogeographic analyses of highly mobile animals with diverse life history are often obscured by long distance re-colonization events and range shifts in dynamically changing environments [1–3]. Studies based on model groups with different biological characteristics are needed to test the validity of zoogeographical hypotheses. Molecular systematics should provide a robust phylogeny for zoogeographic studies and the recent progress makes feasible the studies with hundreds to thousands of analyzed species [4–7]. Insects 2018, 9, 154; doi:10.3390/insects9040154 www.mdpi.com/journal/insects Insects 2018, 9, 154 2 of 18 InsectsHere, 2018, 9 net-winged, x FOR PEER REVIEW beetles (Coleoptera: Lycidae) are studied and we focus on the delimitation2 of of18 tribes, and the evaluation of species richness and distribution. We propose that these beetles can serve asover a model 4200 lycid characterized species have by low been dispersal described propensity and most and diverse ecological are uniformityMetriorrhynchini, [8–13]. Platerodini, Altogether, overLycini, 4200 Calopterini, lycid species and have Calochromini, been described each and of most them diverse with at are least Metriorrhynchini, several hundred Platerodini, species [14,15]. Lycini, Calopterini,Net-winged and beetles Calochromini, have been eachreported of them from with forest at leastand severalshrub habitats hundred of species all continents. [14,15]. Net-wingedTheir larvae beetleslive in haveupper been soil reportedlayers rich from in forestorganic and debris, shrub decaying habitats ofroots all continents. in deeper Theirsoil, rotten larvae tree live trunks in upper or soildead layers branches rich in in organic the canopy debris, of decaying rain and roots cloud in deeperforests soil,[8]. Their rotten unique tree trunks complex or dead mandibles branches are in theadapted canopy for of sucking rain and up cloud liquids forests containing [8]. Their rich unique microbial complex life mandibles [8,16,17]. Therefore, are adapted they for suckingare strictly up liquidslimited containingto habitats richwhere microbial moisture life is [available8,16,17]. Therefore,in decaying they organic are strictlysubstances, limited at least to habitats seasonally. where A moistureprolonged is dry available season in considerably decaying organic limits their substances, abundance at least and seasonally. only drought A prolongedtolerant Calochromini dry season considerablyand Lycini occur limits in theirhigher abundance numbers in and such only areas drought [15,18]. tolerant Calochromini and Lycini occur in higherLycidae numbers is inone such of areas morphologically [15,18]. similar soft-bodied elateroid families, a polyphyletic assemblageLycidae earlier is one ofdesignated morphologically as cantharoids similar soft-bodied [19–21]. They elateroid share families, incomplete a polyphyletic sclerotization assemblage [22–24] earlierwhich designatedlimits their as resistance cantharoids to [19desiccation–21]. They due share to incomplete exposed inter-segmental sclerotization [22 membranes,–24] which limits an absent their resistancesub-elytral to cavity, desiccation and duea delicate to exposed cuticle inter-segmental [14,25]. Their membranes, soft integument an absent provides sub-elytral an cavity, inadequate and a delicateframework cuticle for [flight14,25 ].muscles. Their soft Although integument most provides lycids are an winged, inadequate they frameworkfly slowly, forin short flight distances, muscles. Althoughusually avoid most open lycids windy are winged, and sunny they flyplaces slowly, and in re shortmain distances, inactive on usually leaves avoid under open forest windy canopy and sunny[14,26]. places As anda consequence, remain inactive they on leavesare poor under dispersers. forest canopy Sklenarova [14,26]. Aset aal. consequence, [11] showed they that are poorMetriorrhynchini dispersers. Sklenarova only seldom et al.crossed [11] showed sea straits that and Metriorrhynchini Li et al. [27–29] only identified seldom crossedhigh species sea straits turn- andover Li between et al. [27 –geographically29] identified high close species regions turn-over despite between the absence geographically of apparent close regionsdispersal despite barriers. the absenceNeotenic of females apparent further dispersal decrease barriers. the Neotenicdispersal femalespropensity further of some decrease lycids the as dispersal they retain propensity the larval of somemorphology lycids as when they retainmature the [12,13,30–34]. larval morphology Their dispersa when maturel propensity [12,13,30 is –extremely34]. Their limited, dispersal and, propensity despite istheir extremely ancient limited, origin, their and, despiteranges are their very ancient restricted origin, [9,10,13,23]. their ranges are very restricted [9,10,13,23]. TheThe classificationclassification of net-wingedof net-winged beetles beetles remains rema contentiousins contentious and mutually and incompatiblemutually incompatible topologies havetopologies been discovered have been by discovered earlier morphological by earlier andmo molecularrphological analyses and molecular (Figure1)[ analyses14,15,17 ].(Figure Similarly, 1) their[14,15,17]. distribution Similarly, has their not been distribu criticallytion has analyzed. not been The critically aim of thisanalyzed. study isThe to recoveraim of this the phylogenystudy is to ofrecover net-winged the phylogeny beetles with of net-winged currently available beetles with molecular currently data available and to discuss molecular some data not and yet indicatedto discuss relationshipssome not yet inferredindicated from relationships the molecular inferred phylogeny. from the Further, molecular we focusphylogeny. on the distributionFurther, we offocus tribes on andthe distribution try to define of the tribes areas and with try high to define phylogenetic the areas and with alpha-taxonomic high phylogenetic diversity and andalpha-taxonomic estimate the effectivenessdiversity and of estimate dispersal the barriers. effectiveness of dispersal barriers. FigureFigure 1.1.Overview Overview of of net-winged net-winged beetle beetle classification. classification. (A) Kazantsev (A) Kazantsev (2005) [ 17(2005)]; (B) Bocak[17]; (B et) al. Bocak (2008) et [23 al.]; ((2008)C) Kazantsev [23]; (C (2013)) Kazantsev [35]. (2013) [35]. 2. Material and Methods 2.1. Sampling Altogether, 766 samples and ~550 morphospecies were analyzed (Tables 1 and S1). About 1900 sequences were taken from previous studies, e.g., the previous analysis of Lycidae containing 69 species [23] and several taxonomically restricted studies [11–13,18,26–29]. Additional 800 fragments Insects 2018, 9, 154 3 of 18 2. Material and Methods 2.1. Sampling Altogether, 766 samples and ~550 morphospecies were analyzed (Table1 and Table S1). About 1900 sequences were taken