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© The Norwegian Academy of Science and Letters • Zoologica Scripta,

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Whiting, M. F. (2002). Phylogeny of the holometabolous insect orders: molecular evidence.—

Zoologica Scripta

,

31

, 3–15.Phylogenetic relationships among the holometabolous insect orders were reconstructed using18S ribosomal DNA data drawn from a sample of 182 taxa representing all holometabolousinsect orders and multiple outgroups. Parsimony analysis supports the monophyly of all holo-metabolous insect orders except for Coleoptera and Mecoptera. Mecoptera is paraphyleticwith respect to Siphonaptera, which is nested within Mecoptera. Coleoptera is scattered as aparaphyletic assemblage across the tree topology. These data support a monophyletic Halteria(Strepsiptera + Diptera), Amphiesmenoptera (Trichoptera + Lepidoptera), Neuropterida(Neuroptera + (Megaloptera + Raphidioptera)), but Antliophora (Halteria + Mecoptera +Siphonaptera) and Mecopterida (Antliophora + Amphiesmenoptera) are paraphyletic. Thelimitations of using 18S ribosomal DNA as the sole phylogenetic marker for reconstructinginsect ordinal relationships are discussed.

Michael F. Whiting, Department of Zoology, Brigham Young University, Provo, UT 84602, USA.E-mail: [email protected]

Blackwell Science Ltd

Phylogeny of the holometabolous insect orders: molecular evidence

M

ICHAEL

F. W

HITING

Accepted: 5 October 2001

Introduction

Accounting for more than 80% of insect species and morethan 50% of all animal species (Wilson 1988; Kristensen1999), Holometabola is the most diverse and successful groupof terrestrial organisms. Holometabola comprises 11 insectorders, four of which — Coleoptera, Hymenoptera, Dipteraand Lepidoptera — account for over 99% of the speciesdiversity of this group. Mecoptera, Strepsiptera, Megalopteraand Raphidioptera each contain less than 1000 describedspecies, and Trichoptera, Neuroptera and Siphonapteraeach contain less than 4000 species. The monophyly of eachinsect order is relatively well supported by morphologicaldata (Kristensen 1995, 1999; Whiting

et al

. 1997), with theexception of Mecoptera which appears to be paraphyleticwith respect to Siphonaptera (see Whiting 2002). Apartfrom Holometabola itself, Amphiesmenoptera (Lepidoptera +Trichoptera) is the only well-established interordinal relation-ship, being supported by over 15 synapomorphies (Hennig1981; Kristensen 1997; Whiting

et al

. 1997). Other postulatedinterordinal relationships are based on relatively few morph-ological characters or characters of questionable phylogeneticutility. For example, no characters support a firm placementfor Hymenoptera, which has been postulated as sister group to‘Meronida’ (Mecopterida + Neuropterida) (Boudreaux 1979)or to Mecopterida (Kristensen 1991; 1999; Whiting

et al

.1997). While a sister group relationship between Coleopteraand Neuroptera appears to be widely accepted, it is based

on a single character associated with the female ovipositor(Mickoleit 1973; Achtelig 1975). The highly derived orderSiphonaptera has been associated with Diptera or Mecopterabased on different character suites (Boudreaux 1979; Hennig1981; Kristensen 1991). The most perplexing question, andthat which has received the most attention in recent years,has been the placement of Strepsiptera among the other insectorders. Strepsiptera has been associated with Coleoptera,either within Polyphaga (Crowson 1960) or as sister groupto Coleoptera, based on wing morphology and function(Kristensen 1981, 1991; Kathirithamby 1989; Kukalova-Peck& Lawrence 1993). Detailed examination of these putativesynapomorphies, however, suggests that they are based onmistaken descriptions of strepsipteran wing morphologyand function (Kinzelbach 1990; Pix

et al

. 1993; Whiting 1998b;Beutel & Haas 2000). There have been a number of reviewsof phylogenetically informative characters for Holometabolawith their accompanying phylogenetic hypotheses (Kristensen1975, 1981, 1991, 1995; Boudreaux 1979; Hennig 1981).Whiting

et al

. (1997) presented the first formal quantitativeanalysis of holometabolan relationships based on a codedcharacter matrix and also generated molecular sequence datafrom 18S and 28S ribosomal DNA (rDNA) for Holometabolaand outgroups. The summary topology from the total evidenceanalysis of Whiting

et al

. (1997) is given in Fig. 1. Kristensen(1999) presented an excellent review of holometabolan morph-ology, and his phylogenetic conclusions largely agree with

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Holometabolan phylogeny

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those of Whiting

et al

. (1997), except for uncertainty as towhether Strepsiptera should be placed as sister group toDiptera or Coleoptera.

Given that morphology has led to some ambiguous phylo-genetic relationships within this diverse group, it is notsurprising that in the past few years some effort has beenplaced on using DNA sequence data to decipher interordinalphylogenetic relationships within Holometabola. Carmean

et al

. (1992) sequenced a portion of 18S rDNA from 19 taxarepresenting six holometabolan orders, one hemipteran andone spider outgroup (Fig. 2A). Pashley

et al

. (1993) used 1718S rDNA sequences to represent nine holometabolan ordersand one hemipteran outgroup, and found a monophyleticAmphiesmenoptera and Mecopterida, but other relationshipswere unresolved (Fig. 2B). Chalwatzis

et al

. (1996) sequenced22 exemplars for 18S rDNA to represent nine holometabolanorders and four outgroup taxa (Fig. 2C). Whiting

et al

. (1997)used 87 exemplars for 18S rDNA and 54 exemplars for 28SrDNA to represent all 11 holometabolan orders and 15 out-group orders (Fig. 2D). All of these molecular analyses concurin supporting Amphiesmenoptera (except for Carmean

et al

.1992 who omitted these taxa) and a close association between

Mecoptera and Siphonaptera. The Carmean

et al

. (1992) andChalwatzis

et al

. (1996) analyses suggested a paraphyleticHolometabola, and the Pashley

et al

. (1993) analysis wasunable to test for Holometabola paraphyly. The analysis ofWhiting

et al

. (1997) supported a monophyletic Holometabolaand a sister group relationship between Megaloptera andRaphidioptera. The most intriguing result of these molecularanalyses, and certainly the most controversial, was the evidencepresented for a well-supported sister group relationship betweenStrepsiptera and Diptera (Whiting & Wheeler 1994; Carmean &Crespi 1995; Kristensen 1995; 1999; Whiting & Kathirithamby1995; Huelsenbeck 1997, 1998; Whiting

et al

. 1997; Whiting1998a,b). Beyond the question of phylogenetic affinity of aremarkable group, this result has been centre stage in debatesover competing methods of phylogenetic reconstruction andthe role of a homeotic mutation in giving rise to novel mor-phology in an insect group. A recent summary and re-analysisof holometabolous relationships based on 18S ribosomal datacan be found in Whiting (2001). The analysis in this paper pres-ents a broader selection of taxa, particularly from Coleoptera,than in the Whiting (2001) review, and is thus better able toaddress coleopteran paraphyly based on molecular data.

A. (Hennig)

C. (Whiting) D. (Kristensen)

B. (Boudreaux)

Fig. 1 Previous hypotheses for holometabolan phylogeny. Hennig (A.) (1981), Boudreaux (B.) (1979) and Kristensen (D.) (1999) are basedprimarily on morphological data; Whiting et al. (C.) (1997) is based on a combination of morphological and molecular data. Dotted lines referto poorly supported relationships.


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Materials and methods

18S rDNA sequences were acquired from GenBank andaugmented with sequences generated in the laboratory. Onlysequences with a length of 1 kb or greater were used in thisanalysis, and an attempt was made to represent as many holo-metabolous families as possible. Multiple sequences were usedto represent diverse families (e.g. Carabidae, Scarabaeidae,

Tipulidae), taxa under-represented in previous analyses (e.g.Neuroptera) or taxa whose phylogenetic position is still con-troversial (e.g. Strepsiptera). This sampling strategy resultedin 147 ingroup sequences representing all holometabolousorders and 111 families (Appendix 1). Outgroup taxa wereselected from Paraneoptera, the hypothesized sister group toHolometabola (Whiting

et al

. 1997; Kristensen 1999), and

Fig. 2 Previous molecular hypotheses forHolometabola based on 18S rDNA includingsampled outgroups. Numbers in parenthesesrefer to the number of exemplars used asterminals.



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Polyneoptera (

sensu

Boudreaux 1979), with a sequence fromEphemeroptera used as the most distant outgroup. This resultedin 35 outgroup sequences from 11 orders and 35 families. Ofthe 182 total sequences included in this analysis, 111 wereobtained from GenBank and the remaining 71 were gener-ated in the laboratory using the primers and methodologydescribed in Whiting

et al

. (1997), except that the entire regionof 18S was amplified and sequenced. Roughly two-thirds ofthese sequences consist of the entire region of 18S rDNA andthe other one-third consist of approximately 1 kb of sequencedata. This analysis includes 50 more sequences than in theWhiting (2001) review and represents the broadest selectionof taxa to date for holometabolan phylogeny.

Sequences were assembled in Sequencher™ 3.1.1 (Genecodes1999), and a gross alignment was performed by manuallyaligning the conserved domains across the taxa. Each con-served domain, and variable regions between the domains,were removed in sections and entered into the computerprogram

POY

(Gladstein & Wheeler 1999) to undergo moreexhaustive alignment.

POY

was implemented on a dedicated 32node parallel cluster using gap cost = 2, change cost = 1, withTree Bisection and Reconnection (TBR) branch swapping on100 alignments, with the option ‘implied alignment’ implemented.Although

POY

is designed to construct a topology while

simultaneously performing alignment (Wheeler 1999), theimplied alignment option outputs a multiple alignment whichis more optimal than those typically found by other alignmentalgorithms, such as

MALIGN

(Wheeler & Gladstein 1994) orClustal W (Thompson

et al

. 1994; W. Wheeler, personalcommunication, 2000). The implied alignments generated by

POY

were used as the aligned matrix for phylogenetic analysis.Variable alignment regions which appeared ambiguously

aligned across the insect orders, but relatively conservedwithin each order, were aligned independently within eachholometabolous insect order using

POY

with the parametersas described above. Mecoptera and Siphonaptera were treatedas a single order because previous evidence has suggestedthat Mecoptera is paraphyletic with respect to Siphonaptera(Schlein 1980; Whiting

et al

. 1997; Bilinski

et al

. 1998). Thesevariable regions were excluded from the outgroups becauseresolution among these taxa is not the focus of this study. Eachregion was considered to be an alignment block, and the blockswere assembled into a single matrix by scoring taxa outside ofthe block with missing values. This produces a blocked align-ment for the variable regions, and each of these blocks wasspliced together into a single alignment to form one variableblocked alignment (Fig. 3). The variable blocked regions andconserved regions were then assembled into a single alignment,

Fig. 3 Scheme of alignment for blocked variable regions. Regions that were ambiguously aligned between orders, but unambiguously alignedwithin orders, were aligned as blocks for each holometabolous insect order (represented as light boxes). Taxa outside of the blocked regionswere coded with missing data. These regions were spliced together to create a step-like formation in the total alignment, where the variableblocked regions are flanked by conserved regions. The blocks were combined for Mecoptera and Siphonaptera and excluded for the outgroups.


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with the conserved regions flanking the variable blocked regions.A theoretical justification for this method of alignment hasbeen provided elsewhere (Whiting 2001). The alignment canbe found at http://dnasc.byu.edu/~whitinglab/

.

Trees were reconstructed under parsimony with gaps treatedas missing data. Because of the large size of the data set, anovel method of tree searching was employed. The program

PAUP

* 4.0 (Swofford 2000) was utilized using a implementationof the parsimony ratchet (Nixon 1999) that allows processingon multiple computers in parallel. The parsimony ratchetwas implemented following the general procedure of Nixon(1999) with the following modifications: (i) individual ratchetiterations were parsed to separate machines for computation;(ii) the percentage of reweighted characters was allowed torandomly vary between 5% and 25% for each iteration; (iii) theweight assigned to the random character partition was allowedto randomly vary from 2 to 10 with each iteration; (iv) thecentral CPU distributed a semi-randomized matrix and topo-logy to each nodal CPU for computation; (v) the most optimaltopology from each ratchet iteration was returned to a centralCPU which kept a running tally of all optimal and suboptimaltopologies; and (vi) the central CPU then distributed a newsemi-randomized matrix and optimal topology to the nodalCPUs for computation. A total of 10 000 ratchet iterationswere computed on an average of 256 CPUs. The most optimaltopologies were subjected to TBR branch swapping to enu-merate the entire set of optimal trees. Because the parsimonyratchet more broadly samples the tree landscape than doesthe standard parsimony search technique (Nixon 1999), it islikely that this analysis found a better representation of theentire set of most parsimonious trees than would a standardanalysis. Trees were also computed in

PAUP

* and

NONA

using30 random addition sequences in the former and 100 randomaddition sequences in the latter. In all analyses, the parallelimplementation of the parsimony ratchet found trees that wereshorter than any found using random addition sequences,and these analyses were completed in a few hours in contrastto the many days required for standard

PAUP

* and

NONA

ana-lyses. Bremer support values (Bremer 1994) were calculatedin

NONA

by saving trees up to 10 steps away from the mostparsimonious solution. Bootstrapping was performed in

PAUP

4.0* using a full heuristic search with 100 replicates. Treeswere reconstructed with the blocked variable regions includedand excluded, and Coleoptera was analysed constrained andunconstrained as a monophyletic group.

Results

The alignment of 18S rDNA resulted in 10 conserved regions(regions aligned across all taxa) and three variable regionswhich were blocked as described above. Two highly autapo-morphic strepsipteran insert regions were excluded from theanalysis. Phylogenetic analysis of all aligned data, including

the variable regions, resulted in 4822 trees of length 9353(CI = 0.43, RI = 0.69), the strict consensus of which is pres-ented in Fig. 4. This topology supports a monophyletic Neoptera,but a paraphyletic Paraneoptera (Hemiptera + Thysanoptera +Psocodea), as Psocodea (Phthiraptera + Psocoptera) is placedas the most basal neopteran taxon. Polyneoptera is mono-phyletic and placed as sister group to Hemiptera. WithinPolyneoptera, the monophyly of Orthoptera, Blattoidea,Dictyoptera and Embioptera + Phasmatodea is supported,but Mantodea is paraphyletic. Hemiptera is monophy-letic, as are the suborders Auchenorrhyncha and Heteroptera.Holometabola forms a monophyletic group, although withonly moderate Bremer and bootstrap support values. Allholometabolan orders are supported as monophyletic groups,except for Mecoptera and Coleoptera. In terms of overallrelationships, this analysis divides Holometabola into twomajor clades: (Hymenoptera + (Neuropterida + Mecoptera/Siphonaptera)) and (Amphiesmenoptera + Halteria), withColeoptera scattered as a paraphyletic assemblage through-out the latter clade. These two groups are supported by lowbootstrap and Bremer support values. Antliophora (Diptera +Strepsiptera + Mecoptera + Siphonaptera) is paraphyletic, asis Mecopterida (Antliophora + Amphiesmenoptera).

Hymenoptera is supported as a monophyletic group, butSymphyta and Apocrita are both paraphyletic, and most intra-ordinal relationships are poorly supported. These data supporta monophyletic Neuropterida, with a sister group relation-ship between Raphidioptera and Megaloptera, in agreementwith previous molecular (Whiting

et al

. 1997) and morpho-logical (Kristensen 1999) analyses. However, these resultsdiffer from the conclusions of Aspöck (2002) who placesMegaloptera as sister group to Neuroptera. Within Neurop-terida, Myrmeleontiformia is monophyletic, but it is nestedwithin Hemerobiiformia (Aspöck 1995) making the lattergroup paraphyletic. The monophyly of Hemerobiidae andChrysopidae is also supported in this analysis. Neuroptera isnotoriously difficult to generate reliable ribosomal sequencedata for, because the ribosomal genes in these taxa appear tobe less concerted in their evolution than in other insect groups,and they often include large insert regions that are difficult toamplify and sequence. The sequences included in this studycome primarily from my laboratory, and appear to be authenticin that the same sequence data can be consistently generatedfrom these particular taxa, and the data make sense in thelight of neuropteran phylogeny. More problematic sequencesusing previous analyses (e.g.

Corydalus

and

Agulla

; Whiting

et al.

1997) were excluded from this analysis. Indeed, thedifficulty of generating reliable sequences from a diversity ofneuropteran taxa has made their phylogeny more elusive thanthat of other comparably sized orders.

Mecoptera + Siphonaptera form a relatively well-supportedmonophyletic group. The subordination of Siphonaptera



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within Mecoptera based on 18S rDNA is not a surprise giventhe results of previous molecular analyses. However, theplacement of

Nannochorista

as sister group to the fleas is notsupported in a more extensive molecular and morphologicalanalysis (Whiting 2002), which argues for a sister group rela-tionship with Boreidae. The monophyly of Siphonapteraand Ceratophylloidea (Leptopsyllidae + Ceratophyllidae +Ischnopsyllidae) is well supported. However, phylogeneticrelationships among fleas are poorly known (Lewis & Lewis1985), and so there is no specific morphological hypothesiswith which these molecular data can be readily compared.Within Mecoptera, the monophyly of Panorpomorpha andPanorpiini (Choristidae + (Panorpodidae + Panorpidae)) issupported, but this result disagrees with Willmann (1987) inthe placement of Meropeidae as sister group to Bittacidae,rather than in Opisthogonomorpha.

The second lineage comprises a paraphyletic Coleopteraand a monophyletic Amphiesmenoptera and Halteria.

Archostemata + Myxophaga form the basal-most clade and,although resolution of taxa within Polyphaga is poorly sup-ported, the monophyly of this group is supported with aBremer value of 5. Adephaga is grossly paraphyletic and attachesas two paraphyletic assemblages at two positions on thetopology: basal to Halteria and basal to Amphiesmenoptera.Maddison

et al

. (1999) suggested that the taxa

Omophron

,

Metrius

,

Cicindela

,

Omus

and

Clinidium

had long branchesfor 18S, which may account for their ‘attraction’ (Felsenstein1978) to these other lineages. However, exclusion of thesetaxa from this data set still yields a paraphyletic Coleoptera,with Polyphaga and Adephaga placed far apart on differentportions of the overall topology.

Constraining the monophyly of Coleoptera produces atopology largely congruent with the unconstrained tree forthe non-beetle taxa (Fig. 5). It requires 36 additional stepsto constrain Coleoptera as monophyletic, and an increase of0.4% to the overall tree length. Coleoptera is placed as sister

2

4100

10+

10010+

100

10+

10010+

10010+

100

10+

757

10010+10010+

Archostemata + Myxophaga

Polyphaga

Adephaga

2

12

5

11

22

1

1

1

1

11

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855

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8088544

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804 89

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754

604

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71 171

805 75

3

10010+957

757

10010+

13

10010+

1

10010+ 94

7 703 66

3 955

651

1009

DistocupesHydroscapha

Torridincola

Calopteron

Hololepta

Apatides

Cucujus

AmphotusEleodes

Podabrus

Acmaeodera

Ptinus

ObereaTrox

Trichodes

Coriophorus

Apion

Apoderus

Clambus

Cyphon

Dynastes

Helochares

Ips

Mecomacer

Meloe

Octinodes

Oxycraspedus

Photuris

Platypus

Polydrusus

Rhipiphorus

Tetraopes

Xanthopyga

Xyloryctes

Amphizoa

Copelatus

Haliplus

HygrobiaOmophron

Orectochilus

Suphis

Trachypachus

PycnopsycheHydropsyche

Oxyethira

OecetisBrachycentrus

Wormaldia

Papilio

Hemileuca

Ascalapha

Eriocrania

PrionoxystusPlatyptilia

Galleria

AnthocharisHyles

Agathiphaga

Heterobathmia

Lymantria

Micropteryx

SthenopisTegeticula

Thyridopteryx

Tineola

Lutzomyia

Tanyptera

Dolichopeza

Cicindela

ClinidiumMetrius

Omus

Oxycheila

Caenocholax

Crawfordia

TriozoceraM. chobautiM. chobauti

Elenchus

X. peckiX. vesparum

Stylops

AblabesmyiaDixella

SimuliumCorethrella

Chrysops

MydasLaphria

AnastrephaCeratitis

DrosophilaMythicomyia

Ornithoica

PhlebotomusEpiphragma

Nephrotoma

Holorusia10010+

8

Agulla

AquariusBuenoa

Graphocephalus

Hemiowoodwardia

Hysteropterum

Lygus

Okanagana

OlariusProkelisia

ProsapiaRhaphigaster

Saldula

Scolops

Siphanta

Spissistilus

Cerastipsocus

ColumbicolaMenacanthusNeohaematopinus

Valenzuela

EphemerellaCalopteryxLibellula

Gromphadorhina

Reticulitermes

Paratettix

Stenopelmata

Blaberus

Mantis

OligotomaDiradius

Melanoplus

Pterophylla

Tenodera

Timema

Megarhyssa

Campsomeris

Dolerus

Apoica

Bareogonalos

Caenochrysis

Dasymutilla

Doronomyrmex

Epyris

EvaniaHartigia

Hemitaxonus

Mesopolobus

Monobia

Ophion

Orussus

Polistes

Priocnemus

Trioxys

Apteropanorpa

Bittacus

BoreusCaurinus

Chorista

Merope

Nannochorista

PanorpaBrachypanorpa

Orchopeas

Coptopsylla

MegarthroglossusHystrichopsylla

Myodopsylla

Frontopsylla

Tunga

Acanthopsylla

Polygenis

Craneopsylla

Haplogenius

Eremochrysa

MicromusHemerobius sp.

Anisochrysa

H. stigmata

LolomyiaMantispa

Myrmeleon

Oliarces

Nehga

Sialis

10+

91

10+

100

866

75

5

613

702

603

95

4

Neuropterida

10010+ 95

6809

544

2

1055

957

954

121007 55

11 61

12

754 100

10+1 75

2

1

22 100

9

10010+

903953 95

2

2

1

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703

2

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11005

804

21

14

680

66

1100

10+

100

5903

1

804

1009

742 60

11006

Mecoptera

Neuroptera

Hym

enoptera

Siphonaptera

Trichoptera

Lepidoptera

Strepsiptera

Diptera

Heteroptera

Auchenorrhyncha

Psocodea“Polyneoptera”

Megaloptera

Raphidioptera

Halteria

Amphiesmenoptera

Adephaga

Holometabola

Neoptera

Fig. 4 Strict consensus of 4822 most parsimonious trees (L = 9353, CI = 0.43, RI = 0.69) from the 18S rDNA alignment with blocked variableregions included. Coleoptera and Adephaga are paraphyletic. Numbers above nodes are bootstrap values; numbers below nodes are Bremersupport.


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group to Amphiesmenoptera + Halteria in the constrainedtree, although this is rather poorly supported with low boot-strap and Bremer values. This analysis supports a mono-phyletic Polyphaga (as in the unconstrained tree), but Adephagais unresolved, as are the relationships among the other twocoleopteran suborders.

As in all molecular analyses to date, Amphiesmenopterawas well supported and recovered in this analysis with highBremer and bootstrap values. The monophyly of Lepidopterawas also well supported, although Glossata is paraphyleticwith

Eriocrania

placed as the most basal taxon. The majorityof lepidopteran taxa sampled have only been sequenced forabout 1 kb of 18S, and so inferred relationships may changewith the addition of missing sequence data. Trichoptera wasalso well supported as a monophyletic order, although thesampling of caddisfly taxa was rather sparse.

The controversial group Halteria (Strepsiptera + Diptera)was supported in this analysis. The group was first proposedby Whiting & Wheeler (1994) and subsequently attributedto long-branch attraction (Felsenstein 1978; Carmean &Crespi 1995; Huelsenbeck 1997). I have argued elsewherethat this relationship is most congruent with morphologicaldata, and that it should not be surprising to find sister taxawith elevated substitution rates (Whiting 1998a,b; Sidall &Whiting 1999). Indeed, despite earlier claims that this is theclassic case of long-branch attraction (Huelsenbeck 1997),

re-analysis of the more extensive Whiting

et al

. (1997) dataset by Huelsenbeck (1998), with likelihood methods thataccount for rate heterogeneity, could neither support norrefute this hypothesized sister group relationship. Hwang

et al

.(1998) approached the ‘Strepsiptera problem’ by generatingsequence data for a portion of 28S and 5.8S for a small sampleof holometabolous taxa (11 exemplars). They found that thesedata supported Halteria when analysed via parsimony, butthat they did not support Halteria when analysed via maxi-mum likelihood, and attributed this result to long-branchattraction. However, as their data in fact supported no inter-ordinal holometabolous relationships (as indicated by theirfully unresolved consensus cladogram for holometabolanphylogeny), they were unable to retrieve even those groupswell supported in other molecular and morphological ana-lyses. These results add very little towards decipheringholometabolous relationships, much less the phylogeneticposition of Strepsiptera. Regardless of what side one happensto take in the Strepsiptera controversy, it is clear that addi-tional data are needed to put the issue to rest. The currentanalysis includes two species of what is presumed to be themost primitive strepsipteran genus

Mengenilla

, although inthis analysis they are not placed as the basal-most strep-sipteran taxon. Within Diptera, Brachycera, Cyclorrhaphaand Tipulidae are all well-supported monophyletic groups,but Nematocera is paraphyletic.

When the variable blocked alignment regions are excludedfrom the analysis and only the conserved regions areretained, the same general topology of interordinal relation-ships is produced, with the exception that Hymenopteraand Mecoptera + Siphonaptera switch positions on the tree(Fig. 6). Coleoptera is still grossly paraphyletic with thesuborders attaching in the same position as in the entire

Fig. 5 Summary trees based on the strict consensus trees for parsi-mony analysis of 18S rDNA. The conserved region analysis excludedthe variable blocked regions of the alignment, and produced 19 678trees (L = 7152, CI = 0.37, RI = 0.70). The entire region analysisgenerated the topology in Fig. 4. These trees differ in the place-ment of Hymenoptera relative to Mecoptera + Siphonaptera, andthe manner in which Coleoptera is paraphyletic across the overalltopology.

Fig. 6 Strict consensus of the six most parsimonious trees (L = 9389,CI = 0.41, RI = 0.68) from the 18S rDNA alignment with blockedvariable regions included and the Coleoptera forced as monophyletic.Forcing coleopteran monophyly requires 36 additional steps, anincrease of 0.4% to the overall tree length.



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analysis. Removing these blocks reduces resolution withinLepidoptera, Trichoptera and Polyphaga, and changes rela-tionships within Strepsiptera (

Mengenilla

is the most basalgroup) and Mecoptera (

Apteropanorpa

is the most basalmecopteran taxa, excluding Boreidae). Because the overallrelationships are the same between the entire and conservedanalysis, these results are not particularly sensitive to theinclusion/exclusion of blocked variable regions.

Discussion

This analysis includes more than twice the number of taxathan the Whiting

et al

. (1997) analysis, and 50 more taxa thanthe Whiting (2001) analysis, yet the results are very similar tothese other analyses. 18S rDNA sequence data do a reason-ably good job of supporting the monophyly of each holo-metabolous insect order (with the exception of Coleoptera, asdiscussed below), but do a relatively poor job of supportingmost interordinal relationships, particularly those at the deepernodes of the phylogeny. Amphiesmenoptera, Halteria andSiphonaptera + Mecoptera are well supported (Bremer > 4,bootstrap > 95), Raphidioptera + Megaloptera and Neuropteridaare moderately supported (Bremer > 3, bootstrap > 60), butother interordinal relationships are poorly supported. Con-trary to morphological data, there is no evidence from 18S rDNAto support the monophyly of Antliophora or Mecopterida.These results also suggest that Siphonaptera is nested withinMecoptera, although the exact position of the fleas relativeto Mecoptera is not well supported with these data. In somecases, the 18S rDNA data elucidate the same basic pattern ofrelationships within each order as supported by other data(e.g. in Lepidoptera, Strepsiptera, Diptera, Siphonaptera andMecoptera), although in two cases the results directly con-tradict other data (Hymenoptera and Coleoptera). Fig. 7.

These results highlight some of the difficulties associatedwith inferring higher level phylogenetic relationships frommolecular data. While it is generally recognized that taxonsampling plays a critical role in phylogeny estimation, par-

ticularly at the higher levels (reviewed in Hillis 1998), thedifficulty of adequately sampling Holometabola has receivedlittle attention. Holometabola encompasses what is the mostspeciose and arguably the most diverse group of organismson Earth, and it is a challenge to adequately sample the diver-sity of this clade. This analysis used 147 ingroup sequencesto represent Holometabola. While this is an improvementover earlier studies, it must be acknowledged that the currentnumber of samples equates to one sequenced species repres-enting the diversity of about 58 000 species (Wilson 1988).Thus one might anticipate that inadequate taxon samplingmay lead to unusual results in the phylogeny, and this may bethe case in the topologies generated above.

The importance of thorough taxon sampling in phylo-genetic estimation is perhaps best illustrated by the status ofColeoptera as based on 18S rDNA studies. In the first suchstudy, Coleoptera was represented by a single sequencemaking it impossible to test for beetle monophyly (Carmean

et al

. 1992). In a second study, Coleoptera was representedby two sequences from a single polyphagan superfamily,and resulted in Coleoptera forming a monophyletic group(Chalwatzis

et al

. 1996). It now appears that this presumablycorrect answer was an artifactual result of including only twoexemplars of a single superfamily. Indeed, this analysis was arelatively weak test of beetle monophyly because the diversityof the order was not characterized as broadly as it might havebeen with one exemplar from each of the major suborders.Two 18S rDNA studies have done an admirable job of rep-resenting Adephaga and Polyphaga, although neither studyspecifically tested for coleopteran monophyly, and they lackedthe proper outgroup selection to do so. In the study of Adephaga,the tree was rooted only to Neuropterida (represented by fivesequences; Maddison

et al

. 1999) on the assumption that thissister group relationship was well supported by morphology,although it is based on a single character suite which may ormay not be reliable (Mickoleit 1973; Whiting

et al

. 1997). Inthe study of Polyphaga, the tree was rooted to other beetletaxa from within Polyphaga (Farrell 1998), and so beetle mono-phyly could not be tested. However, as demonstrated above(in agreement with Whiting

et al

. 1997 and Caterino

et al

.2002), when a wide range of beetle and outgroup taxa areincluded, the disturbing result is a paraphyletic Coleoptera,generally with Polyphaga forming one clade and Adephagaforming another, but each placed apart on the topology. WhileI agree with Hennig (1981) that ‘the Coleoptera are as wellfounded a monophyletic group that we could ever hope tofind’ (p. 300), the point is that the current 18S rDNA data donot actually support a monophyletic Coleoptera, althoughunder some sampling strategies and in some analyses theyhave appeared to do so. This lack of support may be duein large part to the difficulty of adequately representingcoleopteran diversity in a molecular phylogenetic study, at

Fig. 7 Summary tree for holometabolan phylogeny based only on 18SrDNA. Dotted lines refer to portions of the topology poorly supportedby the molecular data.


M. F. Whiting

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31

, 1, February 2002, pp3–15

11

least with 18S rDNA. It is tempting to think that the inclusionof additional taxa would remedy this problem, and it may dojust that, but it is also possible that Coleoptera are so diversethat it does not matter how many taxa are sampled, the groupwill always be paraphyletic when relationships are inferredfrom 18S rDNA. Notice, however, that other insect orderswhich are also very large (Lepidoptera and Hymenoptera)are supported as monophyletic with the current 18S rDNAdata, so one cannot simply conclude that large and diverseinsect groups cannot be supported as monophyletic with 18SrDNA data.

One of the frustrations of current insect ordinal system-atics is that the information recovered from molecular datais more redundant with the information from other sourcesthan we would prefer. While, on the one hand, it is comfort-ing that the molecular data recover the monophyly of mostinsect orders, on the other hand these monophyletic groupswere already well supported and the monophyly of most ofthem has never really been in doubt. It is the interordinalrelationships that we are interested in, and they seem to bethe most difficult to extract from the current molecular datawith any degree of confidence. Perhaps the greatest problemin this study, and that of many other higher level phylogeneticstudies, is the reliance on a single marker for phylogeneticinference. Systematics seems to have a constant vibrato of thesuperiority of one character system over another, but if thehistory of systematics has taught us only one thing, it is thatsingle character systems are nearly guaranteed to fail, at leastin some portion of the topology. This is true whether oneuses morphology, molecules or developmental data to inferphylogeny. We should not be surprised to find that the 18SrDNA data do a good job on one portion of the topology, butare rather ill-behaved on other portions; why should they per-form differently from any other character system? The futureof insect molecular systematics lies not only in increasing thetaxon size for a particular marker, but increasing the range ofmarkers used in phylogenetic inference. The combination ofcareful taxon sampling and careful analyses will undoubtedlylead to greater insights into the evolution of the most diversegroup of organisms on Earth, the Holometabola.

Acknowledgements

I thank Paige Humphreys, Alison Whiting, Taylor Maxwelland Matthew Gruwell for assistance in generating the sequencedata, and Matthew Terry, Heath Ogden and Jason Cryan forcomments on the manuscript. This work was supported byNSF grants DEB-9615269 and DEB-9806349, and NSFCAREER award DEB-9983195.

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Appendix 1 List of taxa used in the analysis with 18S sequence accession numbers.

Order Family Name 18S

Ephemeroptera Ephemerellidae Ephemerella sp. Walsh 1863 U65107Odonata Calopterygidae Calopteryx maculata (Beauvois 1805) U65108Odonata Libellulidae Libellula pulchella Drury 1773 U65109Embioptera Oligotomidae Oligotoma saundersii (Westwood 1837) U65117Embioptera Teratembiidae Diradius vandykei (Ross 1944) AF423802Phasmida Timematidae Timema knulli Strohecker 1951 AF423806Orthoptera Tettigoniidae Pterophylla camellifolia (Fabricius 1775) AF423804Orthoptera Stenopelmatidae Stenopelmatus sp. Burmeister 1838 AF423792Orthoptera Acrididae Melanoplus sp. Stål 1873 AF423803Orthoptera Tetrigidae Paratettix toltecus (Saussure 1861) AF423791Blattodea Blaberidae Blaberus sp. Serville 1831 U65112Blattodea Blaberidae Gromphadorhina portentosa (Burmeister 1838) AF423763Mantodea Mantidae Tenodera aridifolia (Stoll 1813) AF423805Mantodea Mantidae Mantis religiosa (L. 1758) U65113Isoptera Rhinotermitidae Reticulitermis tibialis Banks 1920 AF423782Phthiraptera Philopteridae Columbicola columbae (L. 1758) AF423794Phthiraptera Menoponidae Menacanthus sp. Neumann 1912 AF423796Phthiraptera Polyplacidae Neohaematopinus sciuri (Mjöberg 1910) AF423798


M. F. Whiting • Holometabolan phylogeny

© The Norwegian Academy of Science and Letters • Zoologica Scripta, 31, 1, February 2002, pp3–15 13

Psocodea Psocidae Cerastipsocus venosus (Burmeister 1839) U65118Psocodea Caeciliusidae Valenzuela sp. Mockford 1979 AF423793Hemiptera Cicadidae Okanagana utahensis Distant 1914 U06478Hemiptera Cercopidae Prosapia plagiata (Say 1823) U16264Hemiptera Cicadellidae Graphocephalus atropunctata (Signoret 1854) U15213Hemiptera Membracidae Spissistilus festinus (Say 1823) U06477Hemiptera Delphacidae Prokelisia marginata Osborn 1914 U09207Hemiptera Cixiidae Olarius hesperinus Van Duzee 1917 U15215Hemiptera Dictyopharidae Scolops fumida (Uhler 1891) U15216Hemiptera Issidae Hysteropterum severini Caldwell & DeLong 1948 U15214Hemiptera Flatidae Siphanta acuta (Walker 1851) U06481Hemiptera Peloridiidae Hemiowoodwardia wilsoni (Say 1825) AF131198Hemiptera Gerridae Aquarius remigis (Say 1823) U15691Hemiptera Saldidae Saldula pallipes (Fabricius 1794) U65121Hemiptera Notonectidae Buenoa sp. Kirkaldy 1904 U65120Hemiptera Lygaeidae Lygus lineolaris (Palisot 1832) U65122Hemiptera Pentatomidae Rhaphigaster nebulosa (Poda 1865) X89495Coleoptera Cupedidae Distocupes sp. Neboiss 1984 AF201421Coleoptera Torrindicolidae Torridincola sp. Spangler 1934 AF201420Coleoptera Hydroscaphidae Hydroscapha natans LeConte 1874 AF012525Coleoptera Trachypachidae Trachypachus gibbsii LeConte 1861 AF002808Coleoptera Carabidae Cicindela s. sedecimpunctata Klug 1834 AF012518Coleoptera Carabidae Oxycheila nigroaenea Bates 1914 AF201393Coleoptera Carabidae Metrius contractus Eschscholtz 1829 AF012515Coleoptera Carabidae Clinidium calcaratum LeConte 1870 AF012521Coleoptera Carabidae Omophron obliteratum Horn 1870 AF012513Coleoptera Carabidae Omus californicus Eschscholtz 1829 AF012519Coleoptera Haliplidae Haliplus sp. Latreille 1802 AF199516Coleoptera Hygrobiidae Hygrobia sp. Latreille 1817 AF199523Coleoptera Amphizoidae Amphizoa sp. LeConte 1853 AF199520Coleoptera Noteridae Suphis inflatus (LeConte 1863) AF012523Coleoptera Dytiscidae Copelatus chevrolati Aube 1838 AF012524Coleoptera Gyrinidae Orectochilus sp. Lacordaire 1873 AF199513Coleoptera Hydrophilidae Helochares lividus Mulsant 1844 AF201418Coleoptera Histeridae Hololepta sp. Paykull 1811 AF423765Coleoptera Staphylinidae Xanthopyga cacti Horn 1868 AF002810Coleoptera Scirtidae Cyphon hilaris Klausnitzer 1976 AF201419Coleoptera Clambidae Clambus arnetti Endrody-Younga 1981 AF012526Coleoptera Trogidae Trox sp. Fabricius (1775) AF423774Coleoptera Scarabaeidae Dynastes granti Horn 1870 AF002809Coleoptera Scarabaeidae Xylorcytes faunus Hope 1837 U65127Coleoptera Buprestidae Acmaeodera sp. Eschscholtz 1829 AF423771Coleoptera Elateridae Octinodes sp. Candeze 1863 U65128Coleoptera Elateridae Cardiophorus sp. Eschscholtz 1829 AF423776Coleoptera Lycidae Calopteron sp. Guerin-Meneville 1830 AF423764Coleoptera Lampyridae Photuris pennsylvanica De Geer 1774 U65129Coleoptera Cantharidae Podabrus sp. Westwood 1838 AF423770Coleoptera Bostrichidae Apatides sp. Casey 1898 AF423766Coleoptera Anobiidae Ptinus sp. L. 1767 AF423772Coleoptera Cleridae Trichodes ornatus Say (1823) AF423775Coleoptera Nitidulidae Amphotus sp. Erichson 1843 AF423768Coleoptera Cucujidae Cucujus clavipes Fabricius 1777 AF423767Coleoptera Rhipiphoridae Rhipiphorus fasciatus (Say 1823) U65130Coleoptera Meloidae Meloe proscarabaeus (Linnaeus 1758) X77786Coleoptera Tenebrionidae Eleodes sulcipennis Blaisdell 1909 AF423769Coleoptera Cerambycidae Tetraopes tetropthalmus (Forster 1771) U65131Coleoptera Cerambycidae Oberea sp. Mulsant 1839 AF423773Coleoptera Nemonychidae Mecomacer sp. Kuschel 1954 AF250069


Appendix 1 Continued


Holometabolan phylogeny • M. F. Whiting

14 Zoologica Scripta, 31, 1, February 2002, pp3–15 • © The Norwegian Academy of Science and Letters

Coleoptera Belidae Oxycraspedus cornutus Zimmerman 1994 AF250068Coleoptera Attelabidae Apoderus giraffa Suffrian 1870 AF250065Coleoptera Brentidae Apion sp. Herbst 1797 AF250060Coleoptera Curculionidae Polydrusus sericeus (Schaller 1783) AF250086Coleoptera Platypodidae Platypus sp. Herbst 1793 AF250077Coleoptera Scolytidae Ips grandicollis (Eichhoff 1868) AF250074Megaloptera Sialidae Sialis sp. Latreille 1802 X89497Raphidioptera Raphidiidae Agulla adnixa (Hagen 1861) AF286301Raphidioptera Inoceliidae Nehga inflata (Hagen 1861) AF286272Neuroptera Ithonidae Oliarces clara Banks 1908 AF012527Neuroptera Berothidae Lomamymia texana (Banks 1897) U65134Neuroptera Mantispidae Mantispa pulchella (Banks 1912) U65135Neuroptera Hemerobiidae Hemerobius stigmata Stephens 1835 U65136Neuroptera Hemerobiidae Micromus sp. Rambur 1842 AF423789Neuroptera Hemerobiidae Hemerobius sp. L. 1758 AF423790Neuroptera Chrysopidae Anisochrysa carnea Brauer 1851 X89482Neuroptera Chrysopidae Eremochrysa tibialis Banks 1950 AF423788Neuroptera Ascalaphidae Haplogenius appendiculatus (Fabricius 1793) AF423787Neuroptera Myrmeleontidae Myrmeleon immaculatus De Geer 1773 U65137Hymenoptera Cephidae Hartigia cressonii (Kirby 1882) L10173Hymenoptera Orussidae Orussus thoracicus Ashmead 1898 L10174Hymenoptera Tenthredinidae Hemitaxonus sp. Ashmead 1898 U65150Hymenoptera Tenthredinidae Dolerus sp. Panzer 1801 AF423781Hymenoptera Trigonalyidae Bareogonalos canadensis (Harrington 1896) L10176Hymenoptera Evaniidae Evania appendigaster (Linnaeus 1758) L10175Hymenoptera Ichneumonidae Ophion sp. Fabricius 1798 U65151Hymenoptera Ichneumonidae Megarhyssa sp. Ashmead 1900 AF423779Hymenoptera Braconidae Trioxys pallidus (Haliday 1833) AJ009351Hymenoptera Pteromalidae Mesopolobus sp. Westwood 1833 L10177Hymenoptera Bethylidae Epyris sepulchralis Evans 1969 L10180Hymenoptera Chrysididae Caenochrysis doriae (Gribodo 1874) L10179Hymenoptera Pompilidae Priocnemus oregana Banks 1933 L10181Hymenoptera Mutillidae Dasymutilla gloriosa (Saussure 1868) U65152Hymenoptera Scoliidae Campsomeris sp. Guerin-Meneville 1838 AF423780Hymenoptera Vespidae Apoica sp. (Fabricius 1775) U65153Hymenoptera Vespidae Monobia quadridens (L. 1763) U65154Hymenoptera Formicidae Doronomyrmex kutteri Wheeler 1906 X73274Lepidoptera Micropterigidae Micropterix calthella (L. 1761) AF136883, AF136863Lepidoptera Agathiphagidae Agathiphaga queenslandensis (Grote 1865) AF136884, AF136864Lepidoptera Heterobathmiidae Heterobathmia pseuderiocrania (Peck 1818) AF136887, AF136867Lepidoptera Eriocraniidae Eriocrania semipurpurella (Stephens 1834) AF136886, AF136866Lepidoptera Hepialidae Sthenopis quadriguttatus (Grote 1864) AF136891, AF136871Lepidoptera Prodoxidae Tegeticula yuccasella (Riley 1872) AF136889, AF136869Lepidoptera Psychidae Thyridopteryx ephemeraeformis (Haworth 1803) AF136894, AF136874Lepidoptera Tineidae Tineola bisselliella (Hummel 1823) AF136893, AF136873Lepidoptera Cossidae Prionoxystus robiniae (Peck 1818) AF423783Lepidoptera Pterophoridae Platyptilia sp. Hübner 1825 AF423784Lepidoptera Pyralidae Galleria mellonella (L. 1758) AF286298Lepidoptera Papilionidae Papilio troilus L. 1758 AF286299Lepidoptera Pieridae Anthocharis sara Lucas 1852 AF423785Lepidoptera Saturniidae Hemileuca sp. Walker 1855 AF286273Lepidoptera Sphingidae Hyles lineata (Fabricius 1775) AF423786Lepidoptera Lymantriidae Lymantria dispar (L. 1758) AF136892, AF136872Lepidoptera Noctuidae Ascalapha odourata (L. 1758) U65140Trichoptera Philopotamidae Wormaldia moesta (Banks 1914) AF136881, AF136861Trichoptera Brachycentridae Brachycentrus nigrosoma (Banks 1905) AF136880, AF136860Trichoptera Limnephilidae Pycnopsyche lepida (Hagen 1861) AF286292Trichoptera Limnephilidae Hydropsyche sp. Pictet 1834 AF286291




M. F. Whiting • Holometabolan phylogeny

© The Norwegian Academy of Science and Letters • Zoologica Scripta, 31, 1, February 2002, pp3–15 15

Trichoptera Hydroptilidae Oxyethira dualis Morton 1905 AF423801Trichoptera Leptoceridae Oecetis avara Banks 1895 AF286300Siphonaptera Pulicidae Tunga monositus Barnes & Radovsky 1969 AF286279Siphonaptera Rhopalopsyllidae Polygenis pradoi (Wagner 1937) AF286277Siphonaptera Hystricopsyllidae Hystrichopsylla t. talpae (Curtis 1826) AF286281Siphonaptera Coptopsyllidae Coptopsylla africana Wagner 1932 AF286275Siphonaptera Pygiopsyllidae Acanthopsylla r. rothschildi (Rainbow 1805) AF286283Siphonaptera Stephanocircidae Craneopsylla minerva wolffheugeli (Rothschild 1909) AF286286Siphonaptera Ctenophthalimidae Megarthroglossus divisus (Baker 1898) AF286276Siphonaptera Ischnopsyllidae Myodopsylla palposa (Rothschild 1904) AF286282Siphonaptera Leptopsyllidae Frontopsylla nakagawai Liu, Wu, & Chang 1986 AF286280Siphonaptera Ceratophyllidae Orchopeas sexdentatus (Baker 1904) AF286274Mecoptera Nannochoristidae Nannochorista dipteroides Tillyard 1917 AF334799Mecoptera Boreidae Boreus colouradensis Byers 1955 AF286285Mecoptera Boreidae Caurinus dectes Russell 1979 AF286288Mecoptera Meropeidae Merope tuber Newman 1838 AF286287Mecoptera Bittacidae Bittacus strigosus Hagen 1861 AF286290Mecoptera Apteropanorpidae Apteropanorpa evansi Yeates & Byers 1999 AF286284Mecoptera Choristidae Chorista australis Klug 1838 AF286289Mecoptera Panorpodidae Brachypanorpa carolinensis Banks 1905 AF286296Mecoptera Panorpidae Panorpa takenouchii Miyake 1908 AF286278Diptera Tipulidae Tanyptera dorsalis (Walker 1848) AF286295Diptera Tipulidae Epiphragma fasciapenne (Say 1823) AF286294Diptera Tipulidae Holorusia rubiginosa Loew 1863 AF423778Diptera Tipulidae Dolichopeza subalbipes (Johnson 1909) AF286297Diptera Tipulidae Nephrotoma altissima (Osten Sacken 1877) U48379Diptera Chaoboridae Corethrella wirthi Stone 1968 U49736Diptera Dixidae Dixella cornuta (Johannsen 1923) U48381Diptera Chironomidae Ablabesmyia rhamphe Sublette 1964 U48384Diptera Simuliidae Simulium vittatum Zetterstedt 1838 U48383Diptera Psychodidae Lutzomyia shannoni (Dyar 1929) U48382Diptera Psychodidae Phlebotumus papatasi Franca 1924 AF145187Diptera Tabanidae Chrysops niger Macquart 1838 AF073889Diptera Asilidae Laphria sp. Meigen 1803 AF286293Diptera Mydidae Mydas clavatus (Drury 1773) AF423777Diptera Bombyliidae Mythicomyia atra Cresson 1915 U65158Diptera Tephritidae Ceratitis capitata (Wiedemann 1824) AF096450Diptera Tephritidae Anastrepha sp. (Schiner 1868) U01248, U01249 AF114472, AF187101Diptera Drosophilidae Drosophila melanogaster Meigen 1830 M21017Diptera Hippoboscidae Ornithoica vicina (Walker 1849) AF073888Strepsiptera Mengenillidae Mengenilla chobauti Hofeneder 1910 X89441Strepsiptera Mengenillidae Mengenilla chobauti. 1910 AF423800Strepsiptera Corioxenidae Triozocera mexicana Pierce 1909 U65159Strepsiptera Myrmecolacidae Caenocholax fenyesi Pierce 1909 U65160Strepsiptera Elenchidae Elenchus japonica Esaki & Hashimoto 1931 U65162Strepsiptera Stylopidae Xenos vesparum Rossius 1793 X77784Strepsiptera Stylopidae Stylops melittae Pierce 1909 X89440Strepsiptera Stylopidae Xenos peckii Kirby 1813 U65164Strepsiptera Stylopidae Crawfordia n.sp. U65163




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