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Organisms Diversity & Evolution

, Volume 18, Issue 3, pp 327–339 | Cite as

Multiple origin of flightlessness in Phaneropterinae bushcrickets and redefinition of the tribus Odonturini (Orthoptera: Tettigonioidea: Phaneropteridae)

  • Beata GrzywaczEmail author
  • Arne W. Lehmann
  • Dragan P. Chobanov
  • Gerlind U.C. Lehmann
Open Access
Original Article
  • 703 Downloads

Abstract

The possession of wings and ability to fly are a unifying character of higher insects, but secondary loss of wings is widespread. Within the bushcrickets, the subfamily Phaneropterinae (Orthoptera: Tettigonioidea) comprises more than 2000 predominantly long-winged species in the tropics. However, the roughly 300 European representatives are mainly short-winged. The systematics of these radiations have been unclear, leading to their unreliable formal treatment, which has hindered analysis of the evolutionary patterns of flight loss. A molecular phylogeny is presented for 42 short-winged species and members of all European long-winged genera based on the combined data from three nuclear gene sequences (18S, H3, ITS2). We found four phylogenetic lineages: (i) the first included the short-wing species of the genus Odontura; (ii) a further branch is represented by the South-American short-winged Cohnia andeana; (iii) an assemblage of long-wing taxa with a deep branching pattern includes the members of the tribes Acrometopini, Ducetiini, Phaneropterini, and Tylopsidini; (iv) a large group contained all short-winged taxa of the tribe Barbitistini. Phaneropterinae flightlessness originated twice in the Western Palaearctic, with a number of mainly allo- and parapatrically distributed species of the Barbistini in Southeastern Europe, and the Middle East and a limited number of Odontura species in Northern Africa and Southwestern Europe. Both short-winged lineages are well separated, which makes it necessary to restrict the tribe Odonturini to the West-Palaearctic genus Odontura. Other flightless genera previously included in the Odonturini are placed as incertae sedis until their phylogenetic position can be established.

Keywords

Barbitistini Odonturini Molecular phylogeny Flight loss Wing reduction Brachypterism 

Introduction

Insect flight evolved around 400 million years ago (Grimaldi and Engel 2005; Misof et al. 2014), probably only once (Hovmöller et al. 2002; Misof et al. 2014). This way of moving around was a key evolutionary innovation in insects and is one of the reasons for their success (Engel et al. 2013; Nicholson et al. 2014). Flight is advantageous for dispersal and migration (Bowler and Benton 2005) as it allows the quick exploitation of a wide range of interspersed habitats (Kingsolver and Koehl 1994; Denno et al. 1996; Langellotto and Denno 2001). Well-developed wings enable insects to disperse widely and easily in search of mates, food, and new habitats. In some species, flight is primarily an adaption for dispersal, with important consequences for gene flow, speciation, and evolution. The ability to disperse likely makes a major contribution to the fitness of individuals (Mayhew 2007). Powered flight is energetically costly as individuals have to produce and sustain lift and overcome drag. Reviews of flight costs have revealed an energy partitioning conflict between reproduction and flight, resulting in a trade-off: the so-called oogenesis-flight syndrome (Dixon et al. 1993; Guerra 2011). Even at rest, long-winged insects (capable of flight) need extra energy for their flight muscles (Reinhold 1999) and store metabolic resources as readily available flight fuels (Zera 2005; Zera and Zhao 2006). In contrast, flightless individuals can invest more energy into reproduction (Guerra 2011; Steenman et al. 2015).

The development of wings and ability to fly are characteristic traits of all higher insect orders. Nonetheless, a multitude of insect taxa secondarily lost the ability to fly (Roff 1990, 1994a; Wagner and Liebherr 1992), which is interpreted as an evolutionary adaptation to environmental factors (Roff 1994b; Hodkinson 2005). There have been debates on the evolutionary forces driving the occurrence of regressive traits, including flightlessness in insects (Fong et al. 1995; Lahti et al. 2009). The development of flight organs and their physiological maintenance imposes metabolic costs, and any individual must weigh the benefits of flight against the costs. When dispersal does not bring ecological benefits, flightlessness is the natural consequence; this is the case for cave, subterranean or small island insects, and for phoretic species like fleas (Roff 1990, 1994a; Wagner and Liebherr 1992). Habitat stability in forests also seems to support the evolution of flightlessness (Roff 1994b), at least in females (Hunter 1995; Snaell et al. 2007). Furthermore, short-winged species are common in the temperate zones (north and south) and high mountains of the tropics (Roff 1990). Winglessness in these cases seems to be better explained by the costs, where losing the ability to fly is an adaptation for energy saving in less favorite climates. Regardless of the ecological reasons, flightlessness can boost species diversity (Ikeda et al. 2012) and correlates with relaxed molecular evolution in energy-related mitochondrial genes (Mitterboeck and Adamowicz 2013; Mitterboeck et al. 2017).

The bushcricket or katydid subfamily Phaneropterinae is a suitable taxon for studying the origins of flight loss. This subfamily is the most species-rich group within the Tettigonioidea and has approximately 2500 species distributed worldwide, mostly in the tropics (Cigliano et al. 2018). In line with the general pattern for wing reduction, short-winged Phaneropterinae occur in tropical mountains (Braun 2010; Massa 2015), where brachypterism increases with altitude (Braun 2011). In the Western Palaearctic, the situation is completely different: there are just a few long-winged Phaneropterinae and a very large number of short-winged species. All short-winged Phaneropterinae worldwide were originally placed in the single tribe Odonturini (Brunner von Wattenwyl 1878, 1891). The European perspective made it necessary to separate several genera into the tribe Barbitistini (Bey-Bienko 1954). These have radiated into a vast number of allo- and parapatric species (Lehmann 1998) with moderate to small distribution areas in the Eastern Mediterranean (Bey-Bienko 1954; Heller 1984; Willemse and Heller 1992), comprising around 300 described species in 15 genera (Cigliano et al. 2018). This radiation in the Eastern Mediterranean is linked to extraordinary diversification in acoustic communication systems (Heller 1984, 1990, 2006) and corresponding sensory ecology (Stumpner and Heller 1992; Strauß et al. 2012, 2014). From the plesiomorphic state of bidirectional acoustic communication in Phaneropterinae, where males sing and females answer (Heller et al. 2015), some species within the Barbitistini genus Poecilimon Fischer, 1853 reduced the female’s wings, which thus became non-functional for acoustic communication (Heller 1984, 1992; Heller and von Helversen 1993; Anichini et al. 2017). Furthermore, one species, P. intermedius (Fieber, 1853), has switched to obligate parthenogenesis (Lehmann et al. 2011), which occurs in less than ten bushcricket species worldwide, and also has sensory reduction due to its missing sexual communication (Lehmann et al. 2007; Strauß et al. 2014). The reproduction of the Barbitistini, especially the genus Poecilimon (McCartney et al. 2008, 2010), is well-studied due to the extremely large nuptial gifts transferred during mating (Lehmann 2012). One could speculate that flightlessness is a primer for the extraordinary, large nuptial gifts in this tribe, as variations in the sex that searches for mates (unidirectional versus bidirectional species) correlate with spermatophore size (McCartney et al. 2012). Moreover, no other Orthoptera group has been more intensively studied with respect to chromosomal evolution (both chromosome numbers and structures) (Warchałowska-Śliwa 1998; Warchałowska-Śliwa and Heller 1998; Warchałowska-Śliwa et al. 2000, 2008, 2011, 2013; Grzywacz et al. 2011). Astonishingly, all studies reveal low chromosome differentiation between species and genera (Warchałowska-Śliwa et al. 2013; Grzywacz et al. 2014a) and show small phylogenetic signal. The few published molecular studies on Barbitistini bushcrickets are limited to species groups (Lehmann 1998), included in barcoding analyses (Hawlitschek et al. 2017), or have mainly concentrated on the genera Poecilimon (Ullrich et al. 2010) and Isophya Brunner von Wattenwyl, 1878 (Chobanov et al. 2017). In a previous study, we were unable to clarify the position of the Barbitistini relative to Odonturini, due to restricted taxon sampling (Grzywacz et al. 2014b).

Species that radiated in the Western Mediterranean show low lineage diversification, with 17 taxa placed in the single genus Odontura Rambur, 1838 (Supplementary Table 1). They show little variation in their bidirectional acoustic communication system (Heller 1988; Grzywacz et al. 2014b), with the exception of O. microptera; the tegmina in females of this species do not touch each other; therefore, this species might have secondarily returned to a unidirectional acoustic communication system. However, despite their restricted species number, their chromosome organization is very differentiated, with autosome numbers ranging from 26 to 30 in males and sex chromosomes having evolved multiple times (Warchałowska-Śliwa et al. 2011; Grzywacz et al. 2014b). There is little geographic overlap between the many Barbitistini genera in the east and the genus Odontura in the west (Harz 1969; Heller 1988). To add further complication, a multitude of short-winged genera around the world without geographic overlap and very distinct morphologies are still included in the Odonturini, despite the cautionary comments of Braun (2011) and others (Supplementary Table 2, Cigliano et al. 2018).

Here, we performed a molecular phylogenetic analysis of the flightless West-Palaearctic Barbitistini and Odonturini alongside a diverse subset of long-winged genera, including all European genera. We were also able to include the short-winged Cohnia andeana (Hebard, 1924) from South America. We selected three nuclear genes (small subunit ribosomal RNA gene-18S rDNA, histone 3-H3, internal transcribed spacer 2-ITS2), which have been used successfully to resolve Orthoptera phylogenies (Svenson and Whiting 2004; Jost and Shaw 2006; Ullrich et al. 2010; Mugleston et al. 2013; Song et al. 2015; Chobanov et al. 2017). The present study focuses on the evolutionary origin of flightlessness in Phaneropterinae and clarifies the status of the Odonturini.

Material and methods

Taxon sampling

A total of 101 specimens belonging to 42 species of 17 genera of the Phaneropterinae (Orthoptera, Tettigonioidea) were selected for this study (Table 1). From the tribe Barbitistini, which comprises only short-winged species, we sampled 31 species from 10 out of the 15 genera currently recognized. From the tribe Odonturini, which also only comprises short-winged species, we included four species from the genus Odontura and the tentatively placed South American species Cohnia andeana. We also added six long-winged Phaneropterinae species covering selected genera occurring in the Western Palaearctic and one from East Asia hypothesized to be closely related to Odontura (compare Ragge 1980). Three taxa from the genus Tettigonia Linnaeus, 1758, representing a different bushcricket family (Orthoptera, Tettigonioidea, Tettigoniidae) were selected as the outgroup.
Table 1

Taxonomic information and GenBank accession numbers for taxa included in this study

Voucher

Tribe/Family

Species

Collection locality

GenBank Accesion Numbers

18S

H3

ITS2

 

Barbitistini

     

ani1a

ani2a

 

Ancistrura nigrovittata (Brunner von Wattenwyl, 1878)

Greece, Meteora, Kalambaka

Bulgaria, Blagoevgrad, Maleshevska Mouintains

KM819577

KM819578

KM982077

KM982089

KM981967

KM981968

ann1a

ann2a

Andreiniimon nuptialis (Karny, 1918)

Bulgaria, Haskovo, Glouhite Kamani

Macedonia, Crna Reka Valley, Blashnica

KM819579

KM819580

KM982100

KM982111

KM981969

KM981970

bco1a

Barbitistes constrictus Brunner von Wattenwyl, 1878

Bulgaria, Sliven, Zheravna

KM819588

KM982081

KM981978

boc1a

Barbitistes ocskayi Charpentier, 1850

 

Bulgaria, Vidin, Belogradchik

KM819589

KM982082

KM981979

boc2a

  

Croatia, Istria, Padna

KM819590

KM982083

KM981980

boc2b

 

Croatia, Istria, Padna

KM819591

KM982084

KM981981

bye1a

Barbitistes yersini Brunner von Wattenwyl, 1878

Slovenia, Lipiza

KM819592

KM982085

KM981982

bye1b

 

Slovenia, Lipiza

KM819593

KM982086

KM981983

ikr1a

ikr1b

Isophya kraussii Brunner von Wattenwyl, 1878

Germany, Bavaria

Germany, Bavaria

KM819599

KM819600

KM982093

KM982094

KM981989

KM981990

ima1a

ima1b

Isophya major Brunner von Wattenwyl, 1878

Turkey, Antalya, Kuruçay

Turkey, Antalya, Kuruçay

KM819601

KM819602

KM982095

KM982096

KM981991

KM981992

imv1a

imv1b

imv1c

Isophya mavromoustakisi Uvarov, 1936

Cyprus, Pentadactylos Range

Cyprus, Pentadactylos Range

Cyprus, Pentadactylos Range

KM819603

KM819604

KM819605

KM982097

KM982098

KM982099

KM981993

KM981994

KM981995

imo1a

imo1b

imo2a

imo3a

Isophya modestior Brunner von Wattenwyl, 1882

Slovenia, Gabrce

Slovenia, Gabrce

Bulgaria, Vidin, Belogradchik

Serbia, Novi Sad, Kamenitsa

KM819606

KM819607

KM819608

KM819609

KM982101

KM982102

KM982103

KM982104

KM981996

KM981997

KM981998

KM981999

ine1a

Isophya nervosa Ramme, 1931

Turkey, Kütahya, Tavşanlı

KM819610

KM982105

KM982000

ipa1a

Isophya straubei paucidens Heller, 1988

Turkey, Isparta, Davraz

KM819611

KM982106

KM982001

isu1a

isu1b

Isophya aff. sureyai Ramme, 1951

Turkey, Giresun, Tamdere

Turkey, Giresun, Tamdere

KM819612

KM819613

KM982107

KM982108

KM982002

KM982003

ita1a

Isophya taurica Brunner von Wattenwyl, 1878

Ukraine, S Crimea, Babugan Yayla

KM819614

KM982109

KM982004

ize1a

Isophya zernovi Miram, 1938

Turkey, Artvin, Kafkasor

KM819615

KM982110

KM982005

lal1a

lal1b

lal2a

lal2b

Leptophyes albovittata (Kollar, 1833)

Russia, Semibalki

Russia, Semibalki

Russia, Semibalki

Russia, Semibalki

KM819616

KM819617

KM819618

KM819619

KM982112

KM982113

KM982114

KM982115

KM982006

KM982007

KM982008

KM982009

lbo1a

lbo1b

lbo1c

Leptophyes boscii Fieber, 1853

Croatia, Istria, Buje

Croatia, Istria, Buje

Croatia, Istria, Buje

KM819620

KM819621

KM819622

KM982116

KM982117

KM982118

KM982010

KM982011

KM982012

ldi1a

ldi1b

Leptophyes discoidalis (Frivaldszky, 1868)

Serbia, Novi Sad, Kamenica

Serbia, Novi Sad, Kamenica

KM819623

KM819624

KM982119

KM982120

KM982013

KM982014

lpu1a

lpu1b

lpu2a

lpu2b

lpu2c

Leptophyes punctatissima (Bosc, 1792)

Bulgaria, Varna, Botanical Garden

Bulgaria, Varna, Botanical Garden

Germany, Brandenburg, Stahnsdorf

Germany, Brandenburg, Stahnsdorf

Germany, Brandenburg, Stahnsdorf

Bulgaria, Bourgas, Kovach

Bulgaria, Bourgas, Kovach

Bulgaria, Bourgas, Kovach

KM819625

KM819629

KM819626

KM819627

KM819628

KM819630

KM819631

KM819632

KM982121

KM982126

KM982123

KM982124

KM982125

KM982127

KM982128

KM982129

KM982015

KM982019

KM982016

KM982017

KM982018

KM982020

KM982021

KM982022

lsp1a

lsp1b

lsp1c

mor1a

mor1b

mor1c

Metaplastes ornatus (Ramme, 1931)

Macedonia, Bitola, Konjarska Reka

Macedonia, Bitola, Konjarska Reka

Macedonia, Bitola, Konjarska Reka

KM819633

KM819634

KM819635

KM982130

KM982131

KM982132

KM982023

KM982024

KM982025

pan1a

pan1b

Parapoecilimon antalyaensis Karabag, 1975

Turkey, Antalya

Turkey, Antalya

KM819651

KM819652

KM982150

KM982151

KM982041

KM982042

par1a

par1b

par1c

Phonochorion artvinensis Bey-Bienko, 1954

Turkey, Rize, Ikizdere

Turkey, Rize, Ikizdere

Turkey, Rize, Ikizdere

KM819677

KM819678

KM819679

KM982171

KM982172

KM982173

KM982067

KM982068

KM982069

pam1a

pam1b

pam1c

Poecilimon ampliatus Brunner von Wattenwyl, 1878

Slovenia, Gabrce

Slovenia, Gabrce

Slovenia, Gabrce

KM819648

KM819649

KM819650

KM982147

KM982148

KM982149

KM982038

KM982039

KM982040

pfu1a

Poecilimon fussii Fieber, 1878

Bulgaria, Pleven

KM819664

KM982159

KM982054

pgr1a

pgr1b

pgr1c

Poecilimon gracilis (Fieber, 1853)

Macedonia, Jablanica Mountain

Macedonia, Jablanica Mountain

Macedonia, Jablanica Mountain

KM819666

KM819667

KM819668

KM982161

KM982162

KM982163

KM982056

KM982057

KM982058

pmi1a

Poecilimon miramae Ramme, 1933

Turkey (European part), Kırklareli, Mandrakoy

KM819669

KM982164

KM982059

por1a

por2a

Poecilimon ornatus (Schmidt, 1850)

Macedonia, Nidzhe Mountain

Macedonia, Belasitsa Mountain

KM819671

KM819672

KM981962

KM981963

KM982061

KM982062

pth1c

Poecilimon thoracicus (Fieber, 1853)

Bulgaria, Assenovgrad-Plovdiv

KM819676

KM982170

KM982066

pde1a

pde2a

pde2b

Polysarcus denticauda (Charpentier, 1825)

Bulgaria, Smolyan, Stoykite

Macedonia, Jablanica Mountain, Gorna Belica

Macedonia, Jablanica Mountain, Gorna Belica

KM819653

KM819654

KM819655

KM982152

KM982153

KM982154

KM982043

KM982044

KM982045

pel1a

pel2a

pel2b

Polysarcus zacharovi (Stshelkanovtzev, 1910)

Turkey, Kars, Kars-Horasan road

Turkey, Van, Kuskunkıran pass

Turkey, Van, Kuskunkıran pass

KM819656

KM819657

KM819658

KM982156

KM982157

KM982158

KM982046

KM982047

KM982048

psc1a

Polysarcus scutatus (Brunner von Wattenwyl, 1882)

Greece, Ioannina, Epirus

KM819673

KM982167

KM982063

 

Odonturini

     

oas1a

oas1b

oas1c

 

Odontura (Odonturella) aspericauda Rambur, 1838

Spain, Malaga, Serrania de Ronda

Spain, Malaga, Serrania de Ronda

Spain, Malaga, Serrania de Ronda

KM819636

KM819637

KM819638

KM982134

KM982135

KM982136

KM982026

KM982027

KM982028

oma1a

oma1b

oma1c

Odontura (Odonturella) macphersoni Morales-Agacino, 1943

Spain, Caceres, Puerto de Tornavacas

Spain, Caceres, Puerto de Tornavacas

Spain, Caceres, Puerto de Tornavacas

KM819642

KM819643

KM819644

KM982140

KM982141

KM982142

KM982032

KM982033

KM982034

ost1a

Odontura (Odontura) stenoxypha stenoxypha (Fieber, 1853)

Italy, Sicily, Eraclea Minoa, Riserva Nationale Foce de Fiume del Platani,

KM819645

KM982143

KM982035

ogl1a

ogl2a

ogl3a

Odontura (Odontura) glabricauda (Charpentier, 1825)

Spain, Malaga, Serrania de Ronda

Spain, Caceres, Puerto de Tornavacas

Portugal, Faro, Monte da Rafoia

KM819639

KM819641

KM819640

KM982137

KM982139

KM982138

KM982029

KM982031

KM982030

can1a

can2a

Cohnia andeana (Hebard, 1924)

Peru, Cachapojas

Ecuador, Loja, Catamayo

KM819594

KM819595

KM982087

KM982088

KM981984

KM981985

 

Phaneropterini

     

pfa1a

pfa2a

pfa3a

pfa3b

pfa3c

 

Phaneroptera falcata (Poda, 1761)

Poland, OPN, Kolencin

Poland, Bieżanów

Germany, Brandenburg, Prutzke

Germany, Brandenburg, Prutzke

Germany, Brandenburg, Prutzke

KM819659

KM819660

KM819661

KM819662

KM819663

KM981957

KM981958

KM981959

KM981960

KM981961

KM982049

KM982050

KM982051

KM982052

KM982053

pna1a

Phaneroptera nana Fieber, 1853

Macedonia, Brod Municipality, Slatina

KM819670

KM982165

KM982060

 

Ducetiini

     

dju1a

dju1b

dju1c

 

Ducetia japonica (Thunberg, 1815)

South Korea, Seoul Nowon-ku Chung-Gye

South Korea, Seoul Nowon-ku Chung-Gye

South Korea, Seoul Nowon-ku Chung-Gye

KM819596

KM819597

KM819598

KM982090

KM982091

KM982092

KM981986

KM981987

KM981988

 

Acrometopini

     

ase1a

ase1b

ase1c

 

Acrometopa servillea (Brullé, 1832)

Bulgaria, Haskovo, Ivaylovgrad

Bulgaria, Haskovo, Ivaylovgrad

Bulgaria, Haskovo, Ivaylovgrad

KM819581

KM819582

KM819583

KM982122

KM982133

KM982144

KM981971

KM981972

KM981973

asy1a

asy1b

asy1c

asy2a

Acrometopa syriaca Brunner von Wattenwyl, 1878

Cyprus, Pentadactylos-Range

Cyprus, Pentadactylos-Range

Cyprus, Pentadactylos-Range

Turkey, Antalya, Aspendos

KM819584

KM819585

KM819586

KM819587

KM982155

KM982166

KM982078

KM982080

KM981974

KM981975

KM981976

KM981977

 

Tylopsidini

     

tli1a

tli1b

tli1c

 

Tylopsis lilifolia (Fabricius, 1793)

Italy, Abruzzo, Parco Naturale Regionale Sirente-Velin

Italy, Abruzzo, Parco Naturale Regionale Sirente-Velin

Italy, Abruzzo, Parco Naturale Regionale Sirente-Velin

KM819683

KM819684

KM819685

KM981964

KM981965

KM981966

KM982073

KM982074

KM982075

outgroup

Tettigoniidae

     

tvi1a

Tettigonia viridissima (Linnaeus, 1758)

Bulgaria, Dobrich, Bolata Bay

KM819686

KM982079

KM982076

tcc1a

Tettigonia caudata (Charpentier, 1845)

Turkey, Van, Kuskunkıran pass

KM819682

KM982176

KM982072

tca1a

Tettigonia armeniaca Tarbinsky, 1940

Turkey, Savsat-Ardahan

KM819681

KM982175

KM982071

DNA extractions, PCR amplification, and sequencing

Genomic DNA was extracted from a hind leg of individuals using the NucleoSpin® Tissue kit (Macherey-Nagel, Germany), following the manufacturer’s instructions. Polymerase chain reaction (PCR) was carried out to amplify three nuclear genes: a fragment of the small subunit ribosomal RNA (18S rDNA), histone 3 (H3), and internal transcribed spacer 2 (ITS2). The primers used for the amplifications were 18Sai [5′-CCT GAG AAA CGG CTA CCA CAT C-3′] and 18Sbi [5′-GAG TCT CGT TCG TTA TCG GA-3′] for 18S rDNA (Whiting et al. 1997), H3fwd [5′-ATG GCT CGT ACC AAG CAG ACG GC-3′] and H3rev [5′-ATA TCC TTG GGC ATG ATG GTG AC-3′] for H3 (Colgan et al. 1998), and ITS2-28S [5′-GGA TCG ATG AAG AAC G-3′] and 28S–18S [5′-GCT TAA ATT CAG CGG-3′] for ITS2 (Weekers et al. 2001).

The PCR reaction was performed in a 30-μl reaction volume containing 3.0 μl of 10× PCR buffer, 25 mM MgCl2, 10 mM dNTP mixture, 15 μM forward and reverse primers, 1 μl of genomic DNA, 0.2 μl of Taq DNA polymerase (EURx, Poland), and sterile deionized water. The general PCR profile run on the Thermocycler Mastercycler EP (Eppendorf, Germany) consisted of an initial denaturation step at 95 °C for 4 min, followed by 34 cycles at 95 °C for 30 s, 50 °C for 1 min, and 72 °C for 2 min, and a final extension step of 10 min at 72 °C. The cycling conditions for the 18S rDNA amplification consisted of an initial denaturation for 3 min at 94 °C followed by 30 cycles at 94 °C for 1 min, 51 °C and 72 °C for 1.30 min, with a 10-min final extension at 72 °C. PCR products were purified with the GeneMATRIX PCR/DNA Clean-Up Purification kit (EURx, Poland; following the standard protocol) and were sequenced using the ABI Prism BigDye® Terminator kit version 3.1 (PE Applied Biosystems, Foster City, CA) and ABI 3730XL sequencer. DNA sequences for each gene were deposited in GenBank under the accession numbers listed in Table 1.

Phylogenetic analyses

The obtained nucleotide sequences were aligned and edited in Sequencher v. 4.1 (Gene Codes Corporation). Ambiguously aligned regions were identified following the method proposed by Lutzoni et al. (2000). An unambiguous alignment of a 111 bp portion of ITS2 could not be achieved, similar to the ambiguous characters in those nuclear markers found in a previous study of Phaneropterinae bushcrickets (Ullrich et al. 2010). Therefore, this region was excluded from further analysis. The partition homogeneity test (Farris et al. 1995) implemented in PAUP 4.0a (Swofford 2002) was used to determine the validity of combining 18S, H3, and ITS2 genes into a single analysis.

Phylogenetic inference analyses were conducted using maximum likelihood (ML) and Bayesian inference (BI). Best fit models for ML and BI analyses were calculated in MrModeltest (Nylander 2004) using the Akaike information criterion (AIC). SYM with gamma distribution (SYM + G) represented the best fitting model of nucleotide substitution for the combined datasets. Maximum likelihood (ML) analyses were conducted in PAUP 4.0a. Bootstrap support (BS) was calculated with 1000 replicates. Bayesian analysis was performed in MrBayes v 3.1 (Huelsenbeck and Ronquist 2001; Ronquist and Huelsenbeck 2003) with four independent runs, each having three heated and one cold chain. Analyses were run for 10 million generations with trees sampled every 100 generations. Bayesian posterior probabilities (PP) were calculated using a Metropolis-coupled, Markov Chain Monte Carlo (MCMC) sampling approach. The first 25% of each run was discarded as burn-in. Convergence among the runs was assessed using Tracer v1.5 (Rambaut and Drummond 2009). Figtree (http://tree.bio.ed.ac.uk/software/figtree) was used to visualize the trees. Pairwise genetic distances were calculated in Mega v 6.0 (Tamura et al. 2013).

Results

Sequence data

The final DNA sequence dataset comprised 1177 bp. The sequences of the ITS2 gene (289 bp) were more polymorphic than those of H3 and 18S: for all taxa, 70% of sites were variable and about 40% parsimony informative. The tribe Barbitistini had around 60% of sites variable and 47% parsimony informative for the ITS2. The sequences of the H3 gene (328 bp) were less variable: for all taxa, 47% of sites were variable and 18% parsimony informative. In this case, the tribe Barbitistini had 40% of sites variable and 7% parsimony informative. Sequences for 18S rDNA (560 bp) showed a much lower rate of polymorphism, of just 9% across all taxa with 4% of sites parsimony informative, and for Barbitistini, the values were 3 and 1%, respectively. The partition homogeneity test did not detect significant incongruence between genes; so, our analyses were conducted on the combined dataset. For the rDNA genes, in-group genetic distances within Phaneropterinae tribes were largest in Barbitistini (35%) and Odonturini (34%) (Table 2).
Table 2

Mean pairwise distances within studied tribes of Phaneropterinae calculated from combined three nuclear genes (18S + H3 + ITS2)

Taxa

Mean distance within group (%)

Barbitistini

34.4

Odonturini

33.8

Acrometopini

9.1

Phaneropterini

8.4

Tylopsidini

1.3

Ducetiini

0

Phylogenetic analyses

The analyses of maximum likelihood and Bayesian inference resulted in similar tree topologies (Fig. 1). The Bayesian posterior probability values for the nodes were generally higher than the bootstrap values. The outgroup taxon sampling with the three species of the genus Tettigonia, members of the bushcricket subfamily Tettigoniinae, clearly defined and routed the tree. The phylogenetic analysis divided the subfamily Phaneropterinae into four lineages. The first major lineage (short-wing group I) is the sister group to all the rest and comprises solely the species of the genus Odontura, whose monophyly was supported in all analyses, with a posterior probability of 0.7 and bootstrap values of 68%. Our phylogeny suggests that the short-winged Cohnia andeana from the Andes of South America, tentatively placed within Odonturini (Braun 2011), is phylogenetically separated from Odontura and in our analysis represents the sole species of an additional, New World lineage (short-wing group II), paraphyletic to the rest of the Phaneropterinae. The “long-winged” taxa of Phaneropterinae included in this study do not form a homogenous group: they are separated by long branches and have unresolved basal relationships. The latter aspect shows their distinctiveness and supports their traditional placement in four separate tribes: the Acrometopini, Ducetiini, Phaneropterini, and Tylopsidini. Within the fourth major lineage, members of the species-rich tribe Barbitistini form a well-supported monophyletic lineage (short-wing group III) with 100% posterior probability but low bootstrap values (< 50%). The typically brachypterous groups, especially the Barbitistini and the Odonturini, are well separated, which suggests that these groups lost flight independently of each other.
Fig. 1

Bayesian tree from three nuclear gene analyses as performed in MrBayes. The two values on each branch represent the following: (1) Bayesian posterior probability (PP) and (2) maximum likelihood bootstrap support (BS) (only support values above 50%) as PP/BS

Taxonomic conclusions

Based on our analysis, we restrict the tribe Odonturini Brunner von Wattenwyl, 1878 solely to the West-Palaearctic genus Odontura Rambur, 1838 (Supplement Table S1), well separated from the tribe Barbitistini. Other flightless genera from the Americas, tropical Africa and Papua New Guinea and previously included in Odonturini are placed here as incertae sedis (Supplement Table S2) until their phylogenetic position can be established.

Discussion

The phylogenetic analyses of the sequences of the three nuclear DNA genes created a single most parsimonious tree for the Phaneropterinae. Within this tree, the genus Odontura is a clear monophyletic entity, which can be classified as the tribe Odonturini (Supplementary Table 1). However, the long-lasting inclusion of other short-winged genera from all over the world into the Odonturini is rejected here (Supplementary Table 2). The South American genus Cohnia branches outside the Odonturini, in full agreement with our previous phylogenetic results for this genus (Grzywacz et al. 2014b). The phylogenies of two additional genera formerly placed inside the Odonturini have been analyzed before by Mugleston et al. (2013, 2016). Firstly, the Austrodontura capensis (Walker, 1869) (Naskrecki and Bazelet 2011) from the Fynbos Flora of South Africa branches out with a Madagascan long-winged species Parapyrrhicia dentipes Saussure, 1899 (Mugleston et al. 2016) arbitrarily placed in the Phaneropterini, but certainly belonging to an unnamed tribe (Hemp et al. 2017a). The second genus Monticolaria Sjöstedt, 1910 from the mountain arc of East Africa (Hemp et al. 2009; Massa 2015) clusters deep inside a branch containing a number of long-winged genera, traditionally embedded in the Phaneropterini and Tylopsidini (Mugleston et al. 2016). On the basis of our results in combination with the mentioned molecular phylogenetic studies, we formally restrict the tribe Odonturini to the 17 taxa of the genus Odontura and exclude all other short-winged genera from the Odonturini (see Supplementary Table 2). A future study with more comprehensive coverage from the megadiverse Phaneropterinae might clarify their phylogenetic affinities. The current knowledge suggests that the relatives of the short-winged Phaneropterinae may be best searched for in the fully winged genera of the regions of their occurrence. The wing reduction in Odontura and Cohnia is supposed to have evolved independently as both genera live on different continents, with Odontura in the Western Mediterranean, and Cohnia in the Central Andes of South America.

The Eastern Mediterranean genera form a third, well-supported monophyletic group of flightless species, which corresponds with their classification as the tribe Barbitistini. This tribe or at least a subset of genera belonging to it has been repeatedly supported as a monophyletic group (Mugleston et al. 2013, 2016). All species are short-winged and speciation may well have been related to the limited dispersal capacities in the oro-geographic diverse landscapes of Southeastern Europe and Anatolia (Lehmann 1998). This may have contributed to the sheer number of species (around 300), with little geographic overlap between the closely related taxa (Lehmann 1998; Boztepe et al. 2013; Kaya et al. 2015; Chobanov et al. 2017). Similarly to the western Odonturini, the nearest relatives of the Barbitistini are unknown: they probably also originated from some long-winged species that found refugia in the Eastern Mediterranean and radiated into allo- and parapatrically distributed species. The radiation resulting in the huge species number may be the result of geographic separation (discussed in Lehmann 1998) caused by climate cycles including multiple ice-ages (see Hewitt 2000, 2004). The genus Leptophyes has been repeatedly found to branch with the Poecilimon-cluster (Ullrich et al. 2010; Mugleston et al. 2013, 2016; Grzywacz et al. 2014b), which is also supported here for L. punctatissima. Interestingly, the other three species, Leptophyes albovittata (Kollar, 1833), L. boscii Fieber, 1853 and L. discoidalis (Frivaldszky, 1868), nested in another subgroup. This split is coherent with differences in general morphology and bioacoustic data (Bey-Bienko 1954; Kleukers et al. 2010; Sevgili 2004); however, we leave this question open until more Leptophyes species are studied. The genus Andreiniimon Capra, 1937, based on its overall appearance, used to be related to Leptophyes (Bey-Bienko 1954), but our study found it genetically clustered with Metaplastes Ramme, 1939, Barbitistes Charpentier, 1825, and Ancistrura Uvarov, 1921. Interestingly, highly modified external male genitalia are a shared trait of Ancistrura–Andreiniimon–Barbitistes–Metaplastes, which is coupled to a unique sperm-removal ability in the genus Metaplastes (von Helversen and von Helversen 1991; Foraita et al. 2017). Therefore, the modified external male genitalia might be a synapomorphic character for the group and the overall similarity of Andreiniimon with Leptophyes either results from plesiomorphy or convergent evolution. The genus Isophya, with the second highest species-number (Chobanov et al. 2013, 2017; Grzywacz et al. 2014a), has an ancestral position within the Barbitistini.

The full development of wings is the plesiomorphic character state in the Phaneropterinae. Therefore, it was well expected that the European long-winged genera are rather unrelated, separated by long branching axes. This is in complete agreement with the morphologically classified traditional system, where Acrometopa Fieber, 1853, Ducetia Stål, 1874, Phaneroptera Serville, 1831, and Tylopsis Fieber, 1853 are placed in different tribes (Cigliano et al. 2018). The deep splits between the genera studied here are also supported by a much broader phylogenetic approach (Mugleston et al. 2013, 2016). Interestingly, none of the long-winged genera that currently occur in the Mediterranean region seem to be closely related to the short-winged Odonturini in the Southwest or the short-winged Barbitistini in the Southeast. As concluded by several authors (Braun 2011; Naskrecki and Bazelet 2011; Grzywacz et al. 2014b; Massa 2015), wing size reduction resulting in flightlessness must have occurred multiple times in the Phaneropterinae, which is supported by the recent discovery of the short-winged East African genus Peronurella Hemp, 2017, belonging to the tribe Acrometopini (Hemp et al. 2017b). The conclusions of our study are in line with such a notion and support two evolutionary events within the Western Palaearctic and a probable third in South America. The overall number of times this type of concerted evolution has occurred is obviously higher, as worldwide many more short-winged Phaneropterinae genera of unknown tribal affinities occur (Supplementary Table 2). Based on their distinct appearance, we can easily conclude that the short-winged genera do not form a single worldwide group, and instead likely developed regionally on different continents. Phaneropterinae generally lack genital titillators as a shared character (Vahed et al. 2011; Lehmann et al. 2017), but it occurs independently in central and North American taxa of the Dichopetala group (Cohn et al. 2014; Rocha-Sánchez et al. 2015; Barrientos-Lozano et al. 2016), the South African genus Brinckiella Chopard, 1955 (Naskrecki and Bazelet 2009), and the Asian Letana inflata Brunner von Wattenwyl, 1878 (Heller and Liu 2015). However, the convergent development of titillators is linked to mating-related features such as copulation duration (Vahed et al. 2011; Lehmann et al. 2016) or polyandry (Lehmann et al. 2017), but is not coupled to flightlessness. In conclusion, the evolutionary transition to flightlessness seems to be moderately common in bushcrickets and the five events mentioned in the global analysis by Mugleston et al. (2013) are an underestimation.

Brachypterism can be interpreted to be an evolutionary adaptation resulting from a variety of different environmental conditions. At least three conditions could support flightlessness: first, habitat stability is often an explanation, as dispersal becomes less favorable with increasing stability. The chance of ending up at inferior places after emigration may counter its positive effects, such as outbreeding opportunities. Second, the same is true for isolated habitats, where travel by air is either impossible, like in caves, or dangerous as on islands or mountains (Roff 1990; Wagner and Liebherr 1992). Third, whatever the ecological circumstances, an individual is more likely to disperse when the potential benefits exceed the risks and travel costs (Roff 1984, 1990; Wagner and Liebherr 1992).

In line with the general picture for insects (Roff 1990; Guerra 2011), the loss of flight in tropical bushcrickets occurs predominantly at higher altitudes (Braun 2011), either to save metabolic energy at lower temperatures or because long-distance dispersal provides fewer opportunities to colonize new habitats on mountains than in flat landscapes. However, the situation in the Western Palaearctic needs closer examination. Barbitistini genera have an early seasonal occurrence coupled with a rather short and synchronized life history (Lehmann and Lehmann 2006; Lehmann 2012). This might be a leftover from multiple ice-cycles in which the flightless species adapted to local climates. In line with such a scenario, many species nowadays occur on mountains and abundantly thrive in mesophilic meadows. Alternatively, the pattern of a short and early adult season may allow the species to avoid the hot and dry Mediterranean summers. Chobanov et al. (2017) estimated the common ancestor of Barbitistini to have evolved during the so-called Middle Miocene climatic transition, characterized by a global drop in temperatures and dry climates. The loss of flight and fast life cycle may therefore be connected with the necessity to avoid water loss (Chobanov et al. 2017). For example, the species Poecilimon thessalicus Brunner von Wattenwyl, 1891 is known to suffer from the early onset of the dry Mediterranean summer, which leads to the populations living on the dryer, eastern mountain slopes to have a smaller body size than those on the wetter, western mountain slopes (Lehmann and Lehmann 2008).

Whatever the evolutionary forces that led to the multiple loss of flight, the reduced dispersal capacities have promoted speciation, as in other insects (Ikeda et al. 2012; Vogler and Timmermans 2012; Sota et al. 2014). The overall diversity in Barbitistini with almost 300 species is an impressive example of rapid speciation (Lehmann 1998) within a restricted temporal (Ullrich et al. 2010; Chobanov et al. 2017) and spatial frame (Heller 1984; Willemse and Heller 1992). Thus, it could be speculated that brachyptery in Barbitistini bushcrickets has contributed to the impressive species number—mainly by allopatric separation events during multiple ice-cycles in an oro-geographic diverse landscape (Lehmann 1998).

Conclusion

Based on a phylogenetic reconstruction using three nuclear markers, we found strong evidence for multiple flight loss in Phaneropterinae bushcrickets. In the temperate zone of the Western Palaearctic, flightlessness originated twice. In the first group, the Barbitistini, speciation led to an impressive number of mainly allo- and parapatrically distributed species in Southeastern Europe, Anatolia, and the Middle East. The second group, the Odonturini, occurs as a limited number of species in Southwestern Europe and Northern Africa. Interestingly, the closest relatives of the Odonturini are still unknown but may be best searched for in afro- or asiotropical species, which invaded Europe during a warmer climatic period, while the Barbitistini probably originated from long-winged species found their refugia in the Eastern Mediterranean.

Notes

Acknowledgements

This work was partly supported by a joint research project between the Bulgarian Academy of Sciences and the Polish Academy of Sciences (D.P. Chobanov).

Supplementary material

13127_2018_370_MOESM1_ESM.doc (26 kb)
ESM 1 (DOC 26 kb)
13127_2018_370_MOESM2_ESM.doc (36 kb)
ESM 2 (DOC 36 kb)

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corrected publication July/2018

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Authors and Affiliations

  1. 1.Institute of Systematics and Evolution of Animals, Polish Academy of SciencesKrakowPoland
  2. 2.StahnsdorfGermany
  3. 3.Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of SciencesSofiaBulgaria
  4. 4.Evolutionary Ecology, Department of BiologyHumboldt University BerlinBerlinGermany

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