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Phylogeny and Life History Evolution of Blaberoidea (Blattodea) 29-67 78 (1): 29 – 67 2020

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Phylogeny and Life History Evolution of Blaberoidea (Blattodea) 29-67 78 (1): 29 – 67 2020 ZOBODAT - www.zobodat.at Zoologisch-Botanische Datenbank/Zoological-Botanical Database Digitale Literatur/Digital Literature Zeitschrift/Journal: Arthropod Systematics and Phylogeny Jahr/Year: 2020 Band/Volume: 78 Autor(en)/Author(s): Djernaes Marie, Varadinova Zuzana Kotykova, Kotyk Michael, Eulitz Ute, Klass Klaus-Dieter Artikel/Article: Phylogeny and life history evolution of Blaberoidea (Blattodea) 29-67 78 (1): 29 – 67 2020 © Senckenberg Gesellschaft für Naturforschung, 2020. Phylogeny and life history evolution of Blaberoidea (Blattodea) Marie Djernæs *, 1, 2, Zuzana Kotyková Varadínová 3, 4, Michael Kotyk 3, Ute Eulitz 5, Klaus-Dieter Klass 5 1 Department of Life Sciences, Natural History Museum, London SW7 5BD, United Kingdom — 2 Natural History Museum Aarhus, Wilhelm Meyers Allé 10, 8000 Aarhus C, Denmark; Marie Djernæs * [[email protected]] — 3 Department of Zoology, Faculty of Sci- ence, Charles University, Prague, 12844, Czech Republic; Zuzana Kotyková Varadínová [[email protected]]; Michael Kotyk [[email protected]] — 4 Department of Zoology, National Museum, Prague, 11579, Czech Republic — 5 Senckenberg Natural History Collections Dresden, Königsbrücker Landstrasse 159, 01109 Dresden, Germany; Klaus-Dieter Klass [[email protected]] — * Corresponding author Accepted on February 19, 2020. Published online at www.senckenberg.de/arthropod-systematics on May 26, 2019. Editor in charge: Gavin Svenson Abstract. Blaberoidea, comprised of Ectobiidae and Blaberidae, is the most speciose cockroach clade and exhibits immense variation in life history strategies. We analysed the phylogeny of Blaberoidea using four mitochondrial and three nuclear genes from 99 blaberoid taxa. Blaberoidea (excl. Anaplectidae) and Blaberidae were recovered as monophyletic, but Ectobiidae was not; Attaphilinae is deeply subordinate in Blattellinae and herein abandoned. Our results, together with those from other recent phylogenetic studies, show that the structuring of Blaberoidea in Blaberidae, Pseudophyllodromiidae stat. rev., Ectobiidae stat. rev., Blattellidae stat. rev., and Nyctiboridae stat. rev. (with “ectobiid” subfamilies raised to family rank) represents a sound basis for further development of Blaberoidea systematics. Relationships in Blaberidae are widely incongruent with current classifcation, but more congruent with geographic distribution, with large Afrotropical, Neotropical, and Indo-Malayan clades. We further investigate evolutionary trends and correlations of various life history traits: wing development, body size, microhabitat, mating pattern, ootheca handling, and clutch size. Key words. Blaberidae, Ectobiidae, Attaphilinae, character mapping, character correlation, habitat, wing reduction, body size, clutch size, reproductive behaviour. 1. Introduction Blattodea (cockroaches including termites) includes nae (63), and Anaplectinae (2); 60+ further genera are about 7600 species and is divided into three superfami- not assigned to subfamily (BECCALONI 2014). Blaberidae lies: Blaberoidea, Blattoidea, and Corydioidea. Blaber- is classifed into 12 subfamilies: Blaberinae (23 genera), oidea (Figs. 1B – H, 2) contains nearly half of the spe- Diplopterinae (1), Epilamprinae (47), Geoscapheinae (4), cies and is distributed worldwide. It is classifed in two Gyninae (5), Oxyhaloinae (17), Panchlorinae (5), Pan- families: Ectobiidae, the most speciose blattodean family esthiinae (7), Paranauphoetinae (1), Perisphaerinae (19), (2326 species, Fig. 1B – F, BECCALONI & EGGLETON 2013; Pycnoscelinae (3), and Zetoborinae (14); 23 additional often called ‘Blattellidae’); and Blaberidae, the third most genera are not assigned to subfamily (BECCALONI 2014). speciose family (1201 species, Figs. 1G,H, 2, BECCALONI Members of Blaberoidea have been included in most & EGGLETON 2013; Termitidae is the second most speci- phylogenetic studies of Blattodea or Dictyoptera (which ose family). ROTH (2003a) classifed Ectobiidae in 6 sub- additionally includes Mantodea, the praying mantids), ei- families: Attaphilinae (1 genus), Blattellinae (77 genera), ther using morphological (e.g. MCKITTRICK 1964; GRAND- Ectobiinae (11), Nyctiborinae (10), Pseudophyllodromii- COLAS 1996; KLASS & MEIER 2006), molecular (e.g. IN- ISSN 1863-7221 (print) | eISSN 1864-8312 (online) | DOI: 10.26049/ASP78-1-2020-03 29 Djernæs et al.: Blaberoidea evolution WARD et al. 2007; PELLENS et al. 2007a; DJERNÆS et al. dromiinae. Lack of inclusion in phylogenetic studies also 2012; LEGENDRE et al. 2015; WANG et al. 2017; BOURGUIG- concerns some taxa with aberrant life history, such as the NON et al. 2018; EVANGELISTA et al. 2019), or combined minute myrmecophilous Attaphila, which was classifed data sets (WARE et al. 2008; DJERNÆS et al. 2015). EVAN- in a separate subfamily (Attaphilinae) by ROTH (2003a), GELISTA et al. (2019) included a smaller blaberoid taxon but transferred to Blattellinae by DJERNÆS (2018). sample than other recent studies, but is the frst based on Blattodea exhibit a huge variety of reproductive and a huge transcriptomic data set. These studies have gener- other life history strategies as well as wide ranges of ally agreed on the monophyly of Blaberoidea. However, body size and wing development, and the Blaberoidea DJERNÆS et al. (2015), WANG et al. (2017), and BOURGUIG- make the most signifcant contribution to this diversity. NON et al. (2018), who included the rarely sampled Ana- Cockroaches are found in a range of habitats from tropi- plectinae (Fig. 1A), all placed this group in Blattoidea cal forests over temperate heathlands to deserts, and they (called BLATCI clade in DJERNÆS et al. 2015); DJERNÆS occur in a wide variety of microhabitats, e.g. leaf litter, et al. (2015) excluded Anaplectinae from Ectobiidae and soil, dead wood, ant nests, caves, or up in the canopy Blaberoidea, and ranked it as a family, Anaplectidae. (BELL et al. 2007; LEGENDRE et al. 2014). Body size in All of the aforementioned studies also agreed on the cockroaches ranges from 2.5 mm to 78 mm, with both monophyly of Blaberidae. However, several of the blab- the largest and some of the smallest species belong- erid subfamilies appeared non-monophyletic in previous ing to Blaberoidea (GURNEY 1937, 1959). Wing reduc- studies (Fig. S1), and there is little consensus regarding tion has occurred in many groups of cockroaches, and the relationships among the subfamilies. Points of agree- macropterous, brachypterous, and apterous species occur ment are: (1) some Blaberinae are more closely related in all three superfamilies (Corydioidea, Blattoidea, and to Zetoborinae than to other Blaberinae (e.g. MCKITTRICK Blaberoidea). With regard to reproduction, three basic 1964; LEGENDRE et al. 2014, 2017; BOURGUIGNON et al. mating patterns are known in cockroaches (usually fol- 2018); (2) Panesthiinae is paraphyletic with respect to lowing initial courtship): A) The male raises his wings Geoscapheinae, while Panesthiinae + Geoscapheinae is (if present), the female mounts the male, and the male monophyletic (e.g. LEGENDRE et al. 2014, 2017; LO et al. engages the genitalia while underneath the female, mov- 2016); (3) Oxyhaloinae is monophyletic (e.g. LEGENDRE ing backwards if necessary; the animals then assume an et al. 2014, 2017; BOURGUIGNON et al. 2018). end-to-end position, in which mating is completed. B) For Ectobiidae, even with exclusion of Anaplectinae, The male mounts the female and engages the genitalia monophyly has not been demonstrated and there have from this position before assuming the end-to-end posi- long been indications of its paraphyly with respect to tion. C) No mounting is performed; the male and female Blaberidae (e.g. MCKITTRICK 1964; GRANDCOLAS 1996; engage genitalia directly end to end and remain in this KLASS & MEIER 2006; INWARD et al. 2007; PELLENS et al. position. All three patterns are known in Blaberoidea 2007a; DJERNÆS et al. 2012, 2015; BOURGUIGNON et al. (SRENG 1993). Cockroaches employ several ways of han- 2018; EVANGELISTA et al. 2019). The subfamilies Blattelli- dling their eggs, which are usually assembled in an oo- nae (Fig. 1C,D), Ectobiinae (Fig. 1B), Nyctiborinae, and theca: simply producing and depositing an ootheca (ovi- Pseudophyllodromiinae (Fig. 1E,F) were by and large re- parity A); carrying the ootheca externally until the eggs covered as monophyletic, but this was based on the inclu- hatch (oviparity B); carrying the ootheca internally until sion of very few genera of each. However, MCKITTRICK hatch (ovoviviparity A); not producing an ootheca and (1964), KLASS & MEIER (2006), LEGENDRE et al. (2015), carrying the eggs internally until hatch (ovoviviparity B); and WANG et al. (2017) found Pseudophyllodromiinae to and carrying a (thin-walled) ootheca internally, provid- be non-monophyletic, and MCKITTRICK (1964), DJERNÆS ing substantial nourishment to the developing embryos et al. (2012), BOURGUIGNON et al. (2018), and EVANGELISTA (viviparity). All fve modes occur in Blaberoidea (BELL et al. (2019) found Blattellinae to be non-monophyletic et al. 2007). Cockroaches also exhibit large variation in as one genus disassociated from the remaining blattel- clutch size (number of eggs per ootheca), from 3 to 243 lines. So far, authors have rarely argued for family status eggs, with both extremes occurring in Blaberoidea (ROTH for the various ectobiid subfamilies (but see GRANDCOLAS 1995a; GRANDCOLAS & DELEPORTE 1998). Blaberoidea 1996), mainly due to lack of clarity whether or to what furthermore includes taxa with
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