The Insects - Outline of Entomology 3th Edition - Chapter 7 pdf

Although the various groupstaxa, especially the orders, are fairly well defined, the phylogenetic relationships among insect taxa are amatter of much conjecture, even at the level of ord

Tree showing proposed relationships between mosquitoes, midges, and their relatives (After various sources.)

Chapter 7

INSECT SYSTEM ATICS: PHYLOGENY AND

CL A SSIfiCATION

Because there are so many guides to the identity and

classification of birds, mammals, and flowers, it is

tempting to think that every organism in the living

world is known However, if we compared different

books, treatments will vary, perhaps concerning the

taxonomic status of a geographical race of bird, or of

the family to which a species of flowering plant belongs

Scientists do not change and confuse such matters

per-versely Differences can reflect uncertainty concerning

relationships and the most appropriate classification

may be elusive Changes may arise from continuing

acquisition of knowledge concerning relationships,

perhaps through the addition of molecular data to

pre-vious anatomical studies For insects, taxonomy – the

basic work of recognizing, describing, naming, and

classification – is incomplete because there are so many

species, with much variation

The study of the kinds and diversity of organisms

and their inter-relationships – systematics – has been

portrayed sometimes as dull and routine Certainly,

taxonomy involves time-consuming activities,

includ-ing exhaustive library searches and specimen study,

curation of collections, measurements of features from

specimens, and sorting of perhaps thousands of

indi-viduals into morphologically distinctive and coherent

groups (which are first approximations to species), and

perhaps hundreds of species into higher groupings

These essential tasks require considerable skill and are

fundamental to the wider science of systematics, which

involves the investigation of the origin, diversification,

and distribution, both historical and current, of

organ-isms Modern systematics has become an exciting and

controversial field of research, due largely to the

accu-mulation of increasing amounts of nucleotide sequence

data and the application of explicit analytical methods

to both morphological and DNA data, and partly to

increasing interest in the documentation and

preserva-tion of biological diversity

Taxonomy provides the database for systematics

The collection of these data and their interpretation

once was seen as a matter of personal taste, but recently

has been the subject of challenging debate

Entomolo-gical systematists have featured as prominent

parti-cipants in this vital biological enterprise In this chapter

the methods of interpreting relationships are reviewed

briefly, followed by details of the current ideas on a

classification based on the postulated evolutionary

relationships within the Hexapoda, of which the Insecta

forms the largest of four classes

7.1 PHYLOGENETICS

The unraveling of evolutionary history, ics, is a stimulating and contentious area of biology,particularly for the insects Although the various groups(taxa), especially the orders, are fairly well defined, the phylogenetic relationships among insect taxa are amatter of much conjecture, even at the level of orders.For example, the order Strepsiptera is a discrete groupthat is recognized easily by having the fore wingsmodified as balancing organs, yet the identity of itsclose relatives is not obvious Stoneflies (Plecoptera)and mayflies (Ephemeroptera) somewhat resembleeach other, but this resemblance is superficial and mis-leading as an indication of relationship The stonefliesare more closely related to the orthopteroids (cock-roaches, termites, mantids, earwigs, grasshoppers,crickets, and their allies) than to mayflies Resemblancemay not indicate evolutionary relationships Similaritymay derive from being related, but equally it can arisethrough homoplasy, meaning convergent or parallelevolution of structures either by chance or by selectionfor similar functions Only similarity as a result of common ancestry (homology) provides informationregarding phylogeny Two criteria for homology are:

phylogenet-1 similarity in outward appearance, development,composition, and position of features (characters);

2 conjunction – two homologous features (characters)cannot occur simultaneously in the same organism

A test for homology is congruence(correspondence)with other homologies

In segmented organisms such as insects (section2.2), features may be repeated on successive segments,for example each thoracic segment has a pair of legs,and the abdominal segments each have a pair of spir-acles Serial homologyrefers to the correspondence of

an identically derived feature of one segment with thefeature on another segment (Chapter 2)

Traditionally, morphology (external anatomy) vided most data upon which insect relationships werereconstructed Some of the ambiguity and lack of clar-ity regarding insect phylogeny was blamed on inherentdeficiencies in the phylogenetic information provided

pro-by these morphological characters After investigations

of the utility of chromosomes and then differences inelectrophoretic mobility of proteins, molecular sequencedata from the mitochondrial and the nuclear genomeshave become the most prevalent tools used to solvemany unanswered questions, including those con-

cerning higher relationships among insects However,

molecular data are not foolproof; as with all data

sources the signal can be obscured by homoplasy

Nevertheless, with appropriate choice of taxa and

genes, molecules do help resolve certain phylogenetic

questions that morphology has been unable to answer

Another source of useful data for inferring the

phylo-genies of some insect groups derives from the DNA of

their bacterial symbionts For example, the primary

endosymbionts (but not the secondary endosymbionts)

of aphids, mealybugs, and psyllids co-speciate with their

hosts, and bacterial relationships can be used (with

caution) to estimate host relationships Evidently, the

preferred approach to estimating phylogenies is a

holis-tic one, using data from as many sources as possible

and retaining an awareness that not all similarities are

equally informative in revealing phylogenetic pattern

7.1.1 Systematic methods

The various methods that attempt to recover the

pat-tern produced by evolutionary history rely on

observa-tions on living and fossil organisms As a simplification,

three differing methods can be identified: phenetics,

cladistics, and evolutionary systematics

The pheneticmethod (phenetics) relies on estimates

of overall similarity, usually derived from morphology,

but sometimes from behavior and other traits, and

increasingly from molecular evidence Many of those

who have applied phenetics have claimed that

evolu-tion is unknowable and the best that we can hope for

are patterns of resemblance; however, other scientists

believe that the phenetic pattern revealed is as good anestimate of evolutionary history as can be obtained.Alternative methods to phenetics are based on the pre-mise that the pattern produced by evolutionary pro-cesses can be estimated, and, furthermore, ought to

be reflected in the classification Overall similarity, thecriterion of phenetics, may not recover this pattern ofevolution and phenetic classifications are thereforeartificial

The cladisticmethod (cladistics) seeks patterns ofspecial similarity based only on shared, evolutionarilynovel features (synapomorphies) Synapomorphiesare contrasted with shared ancestral features (ple- siomorphies orsymplesiomorphies), which do notindicate closeness of relationship Furthermore, fea-tures that are unique to a particular group (auta- pomorphies) but unknown outside the group do notindicate inter-group relationships, although they arevery useful for diagnosing the group Construction of a

cladogram (Fig 7.1), a treelike diagram portrayingthe phylogenetic branching pattern, is fundamental

to cladistics From this tree, monophyleticgroups, or

clades, their relationships to each other, and a cation, can be inferred directly Sister groupsare taxathat are each other’s closest relatives A monophyletic

classifi-group contains a hypothetical ancestor and all of its

descendants

Further groupings can be identified from Fig 7.1:

paraphyleticgroups lack one clade from amongst thedescendants of a common ancestor, and often are cre-ated by the recognition (and removal) of a derived sub-group; polyphyleticgroups fail to include two or moreclades from amongst the descendants of a common

Phylogenetics 179

Fig 7.1 A cladogram showing the relationships of four species, A, B, C, and D, and examples of (a) the three monophyleticgroups, (b) two of the four possible (ABC, ABD, ACD, BCD) paraphyletic groups, and (c) one of the four possible (AC, AD, BC, andBD) polyphyletic groups that could be recognized based on this cladogram

ancestor (e.g A and D in Fig 7.1c) Thus, when we

recognize the monophyletic Pterygota (winged or

sec-ondarily apterous insects), a grouping of the remainder

of the Insecta, the non-monophyletic “apterygotes”,

is rendered paraphyletic If we were to recognize a

group of flying insects with wings restricted to the

mesothorax (dipterans, male coccoids, and a few

ephemeropterans), this would be a polyphyletic

group-ing Paraphyletic groups should be avoided if possible

because their only defining features are ancestral ones

shared with other indirect relatives Thus, the absence

of wings in the paraphyletic apterygotes is an ancestral

feature shared by many other invertebrates The mixed

ancestry of polyphyletic groups means that they are

biologically uninformative and such artificial taxa

should never be included in any classification

Evolutionary systematicsalso uses estimates of

derived similarity but, in contrast to cladistics,

estim-ates of the amount of evolutionary change are included

with the branching pattern in order to produce a

classification Thus, an evolutionary approach

emphas-izes distinctness, granting higher taxonomic status

to taxa separated by “gaps” These gaps may be created

by accelerated morphological innovation in a lineage,

and/or by extinction of intermediate, linking forms

Thus, ants once were given superfamily rank (the

Formicoidea) within the Hymenoptera because ants

are highly specialized with many unique features that

make them look very different from their nearest

relat-ives However, phylogenetic studies show ants belong

in the superfamily Vespoidea, and are given the rank of

family, the Formicidae (Fig 12.2)

Current classifications of insects mix all three

practices, with most orders being based on groups

(taxa) with distinctive morphology It does not follow

that these groups are monophyletic, for instance

Blattodea, Psocoptera, and Mecoptera almost certainly

are each paraphyletic (see below) However, it is

unlikely that any higher-level groups are polyphyletic

In many cases, the present groupings coincide with

the earliest colloquial observations on insects, for

example the term “beetles” for Coleoptera However, in

other cases, such old colloquial names cover disparate

modern groupings, as with the old term “flies”, now

seen to encompass unrelated orders from mayflies

(Ephemeroptera) to true flies (Diptera) Refinements

continue as classification is found to be out of step with

our developing understanding of the phylogeny Thus,

current classifications increasingly combine traditional

views with recent ideas on phylogeny

7.1.2 Taxonomy and classification

Difficulties with attaining a comprehensive, coherentclassification of the insects arise when phylogeny isobscured by complex evolutionary diversifications.These include radiations associated with adoption ofspecialized plant or animal feeding (phytophagy andparasitism; section 8.6) and radiations from a singlefounder on isolated islands (section 8.7) Difficultiesarise also because of conflicting evidence from immat-ure and adult insects, but, above all, they derive fromthe immense number of species (section 1.3.2)

Scientists who study the taxonomy of insects – i.e.describe, name, and classify them – face a dauntingtask Virtually all the world’s vertebrates are described,their past and present distributions verified and theirbehaviors and ecologies studied at some level In con-trast, perhaps only 5 –20% of the estimated number

of insect species have been described formally, let alonestudied biologically The disproportionate allocation oftaxonomic resources is exemplified by Q.D Wheeler’sreport for the USA of seven described mammal speciesper mammal taxonomist in contrast to 425 describedinsects per insect taxonomist These ratios, which prob-ably have worldwide application, become even morealarming if we include estimates of undescribed species.There are very few unnamed mammals, but estimates

of global insect diversity may involve millions of scribed species

unde-Despite these problems, we are moving towards aconsensus view on many of the internal relationships ofInsecta and their wider grouping, the Hexapoda Theseare discussed below

7.2 THE EXTANT HEXAPODA

The Hexapoda (usually given the rank of superclass)contains all six-legged arthropods Traditionally, theclosest relatives of hexapods have been considered to bethe myriapods (centipedes, millipedes, and their allies).However, as shown in Box 7.1, molecular sequenceand developmental data plus some morphology (espe-cially of the compound eye and nervous system) sug-gest a more recent shared ancestry for hexapods andcrustaceans than for hexapods and myriapods

Diagnostic features of the Hexapoda include the possession of a unique tagmosis(section 2.2), which isthe specialization of successive body segments thatmore or less unite to form sections or tagmata, namely

Box 7.1 Relationships of the Hexapoda to other Arthropoda

The immense phylum Arthropoda, the joint-legged

animals, includes several major lineages: the myriapods

(centipedes, millipedes, and their relatives), the

che-licerates (horseshoe crabs and arachnids), the

crus-taceans (crabs, shrimps, and relatives), and the

hexapods (the six-legged arthropods – the Insecta and

their relatives) The onychophorans (velvet worms,

lobopods) have been included in the Arthropoda, but

are considered now to lie outside, amongst probable

sister groups Traditionally, each major arthropod

lin-eage has been considered monophyletic, but at least

some investigations have revealed non-monophyly of

one or more groups Analyses of molecular data (some

of which were nạve in sampling and analytical methods)

suggested paraphyly, possibly of myriapods and/or

crustaceans Even accepting monophyly of arthropods,

estimation of inter-relationships has been contentious

with almost every possible relationship proposed by

someone A once-influential view of the late Sidnie

Manton proposed three groups of arthropods, namely

the Uniramia (lobopods, myriapods, and insects,

united by having single-branched legs), Crustacea, and

Chelicerata, each derived independently from a

differ-ent (but unspecified) non-arthropod group More recdiffer-ent

morphological and molecular studies reject this

hypo-thesis, asserting monophyly of arthropodization,

although proposed internal relationships cover a range

of possibilities Part of Manton’s Uniramia group – the

Atelocerata (also known as Tracheata) comprising

myriapods plus hexapods – is supported by some

morphology These features include the presence (in

at least some groups) of a tracheal system, Malpighian

tubules, unbranched limbs, eversible coxal vesicles,

postantennal organs, and anterior tentorial arms

Fur-thermore, there is no second antenna (or homolog)

as seen in crustaceans Proponents of this myriapod

plus hexapod relationship saw Crustacea either

group-ing with the chelicerates and the extinct trilobites,

dis-tinct from the Atelocerata, or forming its sister group in

a clade termed the Mandibulata In all these schemes,

the closest relatives of the Hexapoda always were the

Myriapoda or a subordinate group within Myriapoda

In contrast, certain shared morphological features,including ultrastructure of the nervous system (e.g

brain structure, neuroblast formation, and axon

devel-opment), the visual system (e.g fine structure of the

ommatidia, optic nerves), and developmental

pro-cesses, especially segmentation, argued for a closer

relationship of Hexapoda to Crustacea Such a

group-ing, termed the Pancrustacea, excludes myriapods

Molecular sequence data alone, or combined with

morphology, tend to support Pancrustacea over

Atelocerata However, not all analyses actually recover

Pancrustacea and certain genes evidently fail to retainphylogenetic signal from what was clearly a veryancient divergence

If the Pancrustacea hypothesis of relationship is correct, then features understood previously to supportthe monophyly of Atelocerata need re-consideration.Postantennal organs occur only in Collembola andProtura in Hexapoda, and may be convergent with similar organs in Myriapoda or homologous with thesecond antenna of Crustacea The shared absence offeatures such as the second antenna provides poor evidence of relationship Malpighian tubules of hexapodsmust exist convergently in arachnids and evidence forhomology between their structure and development

in hexapods and myriapods remains inadequately studied Coxal vesicles are not always developed andmay not be homologous in the Myriapoda and thoseHexapoda (apterygotes) possessing these structures.Thus, morphological characters supporting Ateloceratamay be non-homologous and may have been conver-gently acquired in association with the adoption of aterrestrial mode of life

A major finding from molecular embryology is that thedevelopmental expression of the homeotic (develop-

mental regulatory) gene Dll (Distal-less) in the mandible

of studied insects resembled that observed in sampledcrustaceans This finding refutes Manton’s argumentfor arthropod polyphyly and the claim that hexapodmandibles were derived independently from those ofcrustaceans Data derived from the neural, visual, anddevelopmental systems, although sampled across few taxa, may reflect more accurately the phylogenythan did many earlier-studied morphological features.Whether the Crustacea in totality or a componentthereof constitute the sister group to the Hexapoda isstill debatable Morphology generally supports a mono-phyletic Crustacea, but inferences from some mole-cular data imply paraphyly, including a suggestion thatMalacostraca alone form the sister taxon to Hexapoda.Given that analysis of combined morphological andmolecular data supports monophyly of Crustacea andPancrustacea, a single origin of Crustacea seems mostfavored Nonetheless, some data imply a quite radicallydifferent relationship of Collembola to Crustacea,implying a polyphyletic Hexapoda In this view, aberrantcollembolan morphology (entognathy, unusual abdom-inal segmentation, lack of Malpighian tubules, singleclaw, unique furcula, unique embryology) derives from

an early-branching pancrustacean ancestry, with restriality acquired independently of Hexapoda Such aview deserves further study – evidently there remainmany questions in the unraveling of the evolution of theHexapoda and Insecta

ter-Phylogenetics 181

Fig 7.2 Cladogram of postulated relationships of extant hexapods, based on combined morphological and nucleotide sequence

data Italicized names indicate paraphyletic taxa Broken lines indicate uncertain relationships Thysanura sensu lato refers to

Thysanura in the broad sense (Data from several sources.)

the head, thorax, and abdomen The head is composed

of a pregnathal region (usually considered to be three

segments) and three gnathal segments bearing

mand-ibles, maxillae, and labium, respectively; the eyes are

variously developed, and may be lacking The thorax

comprises three segments, each of which bears one pair

of legs, and each thoracic leg has a maximum of six

segments in extant forms, but was primitively

11-segmented with up to five exites(outer appendages of

the leg), a coxal endite(an inner appendage of the leg)

and two terminal claws The abdomen originally had

11 segments plus a telson or some homologous

struc-ture; if abdominal limbs are present, they are smaller

and weaker than those on the thorax, and primitively

were present on all except the tenth segment

The earliest branches in the hexapod phylogeny

undoubtedly involve organisms whose ancestors were

terrestrial (non-aquatic) and wingless However, any

combined grouping of these taxa is not monophyletic,

being based on evident symplesiomorphies or

other-wise doubtfully derived characters Included orders

are Protura, Collembola, Diplura, Archaeognatha, and

Zygentoma (= Thysanura) The Insecta proper

com-prise Archaeognatha, Zygentoma, and the huge

radi-ation of Pterygota (the primarily winged hexapods) As

a consequence of the Insecta being ranked as a class,

the successively more distant sister groups Diplura,

Collembola, and Protura, which are considered to be of

equal rank, are treated as classes

Some relationships among the component taxa

of Hexapoda are uncertain, although the cladograms

shown in Figs 7.2 and 7.3, and the classification

pres-ented in the following sections reflect our current

syn-thetic view Previously, Collembola, Protura, and Diplura

were grouped as “Entognatha”, based on resemblance

in mouthpart morphology Entognathan mouthparts

are enclosed in folds of the head, in contrast to

mouth-parts of the Insecta (Archaeognatha + Zygentoma +

Pterygota) which are exposed (ectognathous) However,

two different types of entognathy have been

recog-nized, one type apparently shared by Collembola and

Protura, and the second seemingly unique to Diplura

Other morphological evidence and some molecular

data analyses indicate that Diplura may be closer to

Insecta than to the other entognathans, rendering

Entognatha paraphyletic (as indicated by broken lines

in Fig 7.3) Some highly controversial studies

indic-ate derivation of Collembola (and perhaps Protura)

from within the Crustacea, independently from other

hexapods

7.3 PROTURA (PROTURANS), COLLEMBOLA (SPRINGTAILS), AND DIPLURA (DIPLURANS) 7.3.1 Class and order Protura (proturans)

(see also Box 9.2)Proturans are small, delicate, elongate, mostly un-pigmented hexapods, lacking eyes and antennae, withentognathous mouthparts consisting of slender mand-ibles and maxillae that slightly protrude from the mouthcavity Maxillary and labial palps are present The thorax is poorly differentiated from the 12-segmentedabdomen Legs are five-segmented A gonopore liesbetween segments 11 and 12, and the anus is terminal.Cerci are absent Larval development is anamorphic,that is with segments added posteriorly during develop-ment Protura either is sister to Collembola, formingEllipura in a weakly supported relationship based onentognathy and lack of cerci, or is sister to all remain-ing Hexapoda

7.3.2 Class and order Collembola (springtails) (see also Box 9.2)

Collembolans are minute to small and soft bodied, oftenwith rudimentary eyes or ocelli The antennae are four-

to six-segmented The mouthparts are entognathous,consisting predominantly of elongate maxillae andmandibles enclosed by lateral folds of head, and lackingmaxillary and labial palps The legs are four-segmented.The abdomen is six-segmented with a sucker-like vent-ral tube or collophore, a retaining hook and a furcula(forked jumping organ) on segments 1, 3, and 4, respect-ively A gonopore is present on segment 5, the anus onsegment 6 Cerci are absent Larval development is epi-morphic, that is with segment number constant throughdevelopment Certain controversial studies suggestthat Collembola may have a different evolutionary origin to the rest of the Hexapoda (see Box 7.1) IfCollembola do belong to the Hexapoda, then they formeither the sister group to Protura comprising the cladeEllipura or alone form the sister to Diplura + Insecta

7.3.3 Class and order Diplura (diplurans)

(see also Box 9.2)Diplurans are small to medium sized, mostly

Protura (proturans), Collembola (springtails), and Diplura (diplurans) 183

unpigmented, possess long, moniliform antennae (like

a string of beads), but lack eyes The mouthparts are

entognathous, with tips of well-developed mandibles

and maxillae protruding from the mouth cavity,

and maxillary and labial palps reduced The thorax is

poorly differentiated from the 10-segmented abdomen

The legs are five-segmented and some abdominal

segments have small styles and protrusible vesicles A

gonopore lies between segments 8 and 9, the anus

is terminal Cerci are slender to forceps-shaped The

tracheal system is relatively well developed, whereas

it is absent or poorly developed in other entognath

groups Larval development is epimorphic, with

seg-ment number constant through developseg-ment Diplura

undoubtedly forms the sister group to Insecta

7.4 CLASS INSECTA (TRUE INSECTS)

Insects range from minute to large (0.2 mm to 30 cm

long) with very variable appearance Adult insects

typically have ocelli and compound eyes, and the

mouthparts are exposed (ectognathous) with the

max-illary and labial palps usually well developed The

thorax may be weakly developed in immature stages

but is distinct in flighted adult stages, associated with

development of wings and the required musculature;

it is weakly developed in wingless taxa Thoracic

legs have more than five segments The abdomen is

primitively 11-segmented with the gonopore nearly

always on segment 8 in the female and segment 9 in

the male Cerci are primitively present Gas exchange

is predominantly tracheal with spiracles present on

both the thorax and abdomen, but may be variably

reduced or absent as in some immature stages

Larval/nymphal development is epimorphic, that is,

with the number of body segments constant during

7.4.1 Archaeognatha and Zygentoma

( Thysanura sensu lato)

Order Archaeognatha (archaeognathans, bristletails) (see also Box 9.3)

Archaeognathans are medium sized, cylindrical, and primitively wingless (“apterygotes”).The head bears three ocelli and large compound eyesthat are in contact medially The antennae are multi-segmented The mouthparts project ventrally, can bepartially retracted into the head, and include elongatemandibles with two neighboring condyles each andelongate seven-segmented maxillary palps Often acoxal style occurs on coxae of legs 2 and 3, or 3 alone.Tarsi are two- or three-segmented The abdomen con-tinues in an even contour from the humped thorax,and bears ventral muscle-containing styles (represent-ing reduced limbs) on segments 2–9, and generally one

elongate-or two pairs of eversible vesicles medial to the styles onsegments 1–7 Cerci are multisegmented and shorterthan the median caudal appendage Developmentoccurs without change in body form

The fossil taxon Monura belongs in Thysanura

Fig 7.3 Cladogram of postulatedrelationships of early-branching hexapod orders, based on morphologicaldata Italicized names indicate likelyparaphyletic taxa Broken lines indicateuncertain relationships (Data fromseveral sources.)

sensu lato The two families of recent Archaeognatha,

Machilidae and Meinertellidae, form an undoubted

monophyletic group The order probably is placed as

the earliest branch of the Insecta, and as sister group

to Zygentoma + Pterygota (Fig 7.3) Alternatively, a

potentially influential recent molecular analysis revived

the concept of Archaeognatha as sister to Zygentoma,

in a grouping that should be called Thysanura (sensu

lato – meaning in the broad sense in which the name

was first used for apterous insects with “bristle tails”)

Order Zygentoma (Thysanura, silverfish)

(see also Box 9.3)

Zygentomans (thysanurans) are medium sized,

dorso-ventrally flattened, and primitively wingless

(“aptery-gotes”) Eyes and ocelli are present, reduced or absent,

the antennae are multisegmented The mouthparts

are ventrally to slightly forward projecting and include

a special form of double-articulated (dicondylous)

mandibles, and five-segmented maxillary palps The

abdomen continues the even contour of the thorax,

and includes ventral muscle-containing styles

(repres-enting reduced limbs) on at least segments 7–9,

some-times on 2–9, and with eversible vesicles medial to

the styles on some segments Cerci are multisegmented

and subequal to the length of the median caudal

appendage Development occurs without change in

body form

There are four extant families Zygentoma is the

sister group of the Pterygota (Fig 7.3) alone, or perhaps

with Archaeognatha in Thysanura sensu lato (see

above under Archaeognatha)

7.4.2 Pterygota

Pterygota, treated as an infraclass, are the winged or

secondarily wingless (apterous) insects, with thoracic

segments of adults usually large and with the

meso-and metathorax variably united to form a pterothorax

The lateral regions of the thorax are well developed

Abdominal segments number 11 or fewer, and lack

styles and vesicular appendages like those of

aptery-gotes Most Ephemeroptera have a median terminal

filament The spiracles primarily have a muscular

closing apparatus Mating is by copulation

Metamor-phosis is hemi- to holometabolous, with no adult

ecdysis, except for the subimago (subadult) stage in

Ephemeroptera

Informal grouping “Palaeoptera”

Insect wings that cannot be folded against the body atrest, because articulation is via axillary plates that are fused with veins, have been termed “palaeopteran”(old wings) Living orders with such wings typicallyhave triadic veins (paired main veins with intercalatedlongitudinal veins of opposite convexity/concavity tothe adjacent main veins) and a network of cross-veins(figured in Boxes 10.1 and 10.2) This wing venationand articulation, together with paleontological studies

of similar features, was taken to imply that Odonataand Ephemeroptera form a monophyletic group,termed Palaeoptera The group was argued to be sister

to Neoptera which comprises all remaining extant andprimarily winged orders However, reassessment ofmorphology of extant early-branching lineages andrecent nucleotide sequence evidence fails to providestrong support for monophyly of Palaeoptera Here wetreat Ephemeroptera as sister group to Odonata +Neoptera, giving a higher classification of Pterygotainto three divisions

Division (and order) Ephemeroptera (mayflies)

(see also Box 10.1)Ephemeroptera has a fossil record dating back to the Carboniferous and is represented today by a fewthousand species In addition to their “palaeopteran”wing features mayflies display a number of uniquecharacteristics including the non-functional, stronglyreduced adult mouthparts, the presence of just one axillary plate in the wing articulation, a hypertrophiedcostal brace, and male fore legs modified for graspingthe female during copulatory flight Retention of asubimago (subadult stage) is unique Nymphs (larvae)are aquatic and the mandible articulation, which isintermediate between monocondyly and the dicondy-lous ball-and-socket joint of all higher Insecta, may

be diagnostic Historic contraction of ephemeropterandiversity and remnant high levels of homoplasy renderphylogenetic reconstruction difficult Ephemeropteratraditionally has been divided into two suborders:Schistonota (with nymphal fore-wing pads separatefrom each other for over half their length) containingsuperfamilies Baetoidea, Heptagenioidea, Leptophle-bioidea, and Ephemeroidea, and Pannota (“fused back”– with more extensively fused fore-wing pads) contain-ing Ephemerelloidea and Caenoidea Recent studiessuggest this concept of Schistonota is paraphyletic, but

no robust alternative scheme has been proposed

Class Insecta (true insects) 185

Division (and order) Odonata (dragonflies and damselflies)

(see also Box 10.2)

Odonates have “palaeopteran” wings as well as many

additional unique features, including the presence of

two axillary plates (humeral and posterior axillary) in

the wing articulation and many features associated

with specialized copulatory behavior, including

posses-sion of secondary copulatory apparatus on ventral

seg-ments 2–3 of the male and the formation of a tandem

wheel during copulation (Box 5.3) The immature

stages are aquatic and possess a highly modified

pre-hensile labium for catching prey (Fig 13.4)

Odonatologists (those that study odonates)

tradi-tionally recognized three groups generally ranked as

suborders: Zygoptera (damselflies), Anisozygoptera

and Anisoptera (dragonflies) Anisozygoptera is minor,

containing fossil taxa but only one extant genus with

two species Assessment of the monophyly or paraphyly

of each suborder has relied very much on

interpreta-tion of the very complex wing venainterpreta-tion Interpretainterpreta-tion

of wing venation within the odonates and between

them and other insects has been prejudiced by prior

ideas about relationships Thus the Comstock and

Needham naming system for wing veins implies that

the common ancestor of modern Odonata was

anisop-teran, and the venation of zygopterans is reduced In

contrast, the Tillyard-named venational system implies

that Zygoptera is a grade (is paraphyletic) to

Aniso-zygoptera, which itself is a grade on the way to a

monophyletic Anisoptera A well-supported view,

incorporating information from the substantial fossil

record, has Zygoptera probably paraphyletic,

Anisozy-goptera undoubtedly paraphyletic, and Anisoptera as

monophyletic sister to some extinct anisozygopterans

Zygoptera contains three broad superfamilial

group-ings, the Coenagrionoidea, Lestoidea, and

Caloptery-goidea Amongst Anisoptera four major lineages can be

recognized, but their relationships to each other are

obscure

Division Neoptera

Neopteran (“new wing”) insects diagnostically have

wings capable of being folded back against their

abdomen when at rest, with wing articulation that

derives from separate movable sclerites in the wing

base, and wing venation with none to few triadic veins

and mostly lacking anastomosing (joining) cross-veins

(Fig 2.21)

The phylogeny (and hence classification) of the

neopteran orders remains subject to debate, mainly

concerning (a) the placement of many extinct ordersdescribed only from fossils of variably adequate pre-servation, (b) the relationships among the Polyneop-tera (orthopteroid plus plecopteroid orders), and (c) the relationships of the highly derived Strepsiptera

Here we summarize the most recent researchfindings, based on both morphology and molecules Nosingle or combined data set provides unambiguous resolution of insect order-level phylogeny and there are several areas of controversy Some questions arisefrom inadequate data (insufficient or inappropriatetaxon sampling) and character conflict within existingdata (support for more than one relationship) In theabsence of a robust phylogeny, ranking is somewhatsubjective and “informal” ranks abound

A group of 11 orders is termed the Polyneoptera (if monophyletic and considered to be sister to theremaining Neoptera) or Orthopteroid–Plecopteroidassemblage (if monophyly is uncertain) The remain-ing neopterans can be divided readily into two mono-phyletic groups, namely Paraneoptera (hemipteroidassemblage) and Endopterygota (= Holometabola).These three clades may be given the rank of subdivi-sion Polyneoptera and Paraneoptera both have ple-siomorphic hemimetabolous development in contrast

to the complete metamorphosis of Endopterygota

Subdivision Polyneoptera (or Orthopteroid– Plecopteroid assemblage)

This grouping comprises the orders Plecoptera, todea, Blattodea, Isoptera, Grylloblattodea, Manto-phasmatodea, Orthoptera, Phasmatodea, Embiidina,Dermaptera, and Zoraptera

Man-Some early-branching events amongst the pteran orders are becoming better understood, butsome relationships remain poorly resolved, and oftencontradictory between those suggested by morphologyand those from molecular data The 11 included ordersmay form a monophyletic Polyneoptera based on the shared presence of tarsal plantulae (lacking only

neo-in Zoraptera) and certaneo-in analyses of nucleotidesequences Within Polyneoptera, the grouping com-prising Blattodea (cockroaches), Isoptera (termites),and Mantodea (mantids) – the Dictyoptera (Fig 7.4) –

is robust All three orders within Dictyoptera share distinctive features of the head skeleton (perforated tentorium), mouthparts (paraglossal musculature),digestive system (toothed proventriculus), and femalegenitalia (shortened ovipositor above a large subgen-

ital plate) which demonstrate monophyly substantiated

by nearly all analyses based on nucleotide sequences

Dermaptera (the earwigs) and Zoraptera (zorapterans)

form an unexpected higher clade based on recent

nucleotide sequence data: some analyses place this

group outside the Polyneoptera as sister to the

remain-ing Neoptera, but the position is best represented as

unresolved at the base of the assemblage (Fig 7.2) The

Grylloblattodea (the ice crawlers or rock crawlers;

now apterous, but with winged fossils) forms a

well-supported clade with the newly established order

Mantophasmatodea

Some data suggested that Orthoptera (crickets,

katy-dids, grasshoppers, locusts, etc.), Phasmatodea

(stick-insects or phasmids), and Embiidina (webspinners)

may be closely related in a grouping called

Orthop-teroidea, although recent investigations suggest an

earlier-branching position for Orthoptera The

rela-tionships of Plecoptera (stoneflies) to other groupings

are poorly understood

Order Plecoptera (stoneflies) (see also Box 10.3)

Plecoptera are mandibulate in the adult, with filiform

antennae, bulging compound eyes, two to three ocelli

and subequal thoracic segments The fore and hind

wings are membranous and similar except that the

hind wings are broader; aptery and brachyptery are

fre-quent The abdomen is 10-segmented, with remnants

of segments 11 and 12 present, including cerci

Nymphs are aquatic

Monophyly of the order is supported by few

mor-phological characters, including in the adult the

looping and partial fusion of gonads and male seminal

vesicles, and the absence of an ovipositor In nymphs

the presence of strong, oblique, ventro-longitudinal

muscles running intersegmentally allowing lateral

undulating swimming, and the probably widespread

“cercus heart”, an accessory circulatory organ

asso-ciated with posterior abdominal gills, support the

mono-phyly of the order Nymphal plecopteran gills may

occur on almost any part of the body, or may be absent.This varied distribution causes problems of homo-logy of gills between families, and between those ofPlecoptera and other orders Whether Plecoptera areancestrally aquatic or terrestrial is debatable The phy-logenetic position of Plecoptera is certainly amongst

“lower Neoptera”, early in the diversification of theassemblage, possibly as sister group to the remainder

of Polyneoptera, but portrayed here as unresolved (Fig 7.2)

Internal relationships have been proposed as twopredominantly vicariant suborders, the austral (south-ern hemisphere) Antarctoperlaria and northernArctoperlaria The monophyly of Antarctoperlaria isargued based on the unique sternal depressor muscle ofthe fore trochanter, lack of the usual tergal depressor,and presence of floriform chloride cells which may have a sensory function Some included taxa are thelarge-sized Eustheniidae and Diamphipnoidae, theGripopterygidae, and Austroperlidae – all southernhemisphere families Some nucleotide sequence studiessupport this clade

The sister group Arctoperlaria lacks defining phology, but is united by a variety of mechanisms asso-ciated with drumming (sound production) associatedwith mate-finding Component families Scopuridae,Taeniopterygidae, Capniidae, Leuctridae, and Nemo-uridae (including Notonemouridae) are essentiallynorthern hemisphere with a lesser radiation of Noto-nemouridae into the southern hemisphere Somenucleotide sequence analyses suggest paraphyly ofArctoperlaria, with most elements of Notonemouridaeforming the sister group to the remainder of the fami-lies Relationships amongst extant Plecoptera havebeen used in hypothesizing origins of wings from “tho-racic gills”, and in tracing the possible development ofaerial flight from surface flapping with legs trailing onthe water surface, and forms of gliding Current views

mor-of the phylogeny suggest these traits are secondary andreductional

Class Insecta (true insects) 187

Fig 7.4 Cladogram of postulated

relationships within Dictyoptera, based

on combined morphological and

nucleotide sequence data The broken

line indicates a paraphyletic taxon

(Data from several sources.)

Order Isoptera (termites, white ants) (see also Box 12.3)

Isoptera forms a small order of eusocial insects with a

polymorphic caste system of reproductives, workers,

and soldiers Mouthparts are blattoid and mandibulate

Antennae are long and multisegmented The fore and

hind wings generally are similar, membranous, and

with restricted venation; but Mastotermes

(Mastoter-mitidae) with complex wing venation and a broad

hind-wing anal lobe is exceptional The male external

genitalia are weakly developed and symmetrical, in

contrast to the complex, asymmetrical genitalia of

Blattodea and Mantodea Female Mastotermes have a

reduced blattoid-type ovipositor

The Isoptera has always been considered to belong in

Dictyoptera close to Blattodea, but precise relationships

have been uncertain A long-held view that

Mastoter-mitidae is the earliest extant branch in the Isoptera

is upheld by all studies – the distinctive features

men-tioned above evidently are plesiomorphies Recent

studies that included structure of the proventriculus

and nucleotide sequence data suggest that termites

arose from within the cockroaches, thereby rendering

Blattodea paraphyletic (Fig 7.4) Under this scenario,

the (wingless) woodroaches of North America and

eastern Asia (genus Cryptocercus) are sister group to

Isoptera Alternative suggestions of the independent

origin (hence convergence) of the semisociality

(par-ental care and transfer of symbiotic gut flagellates

between generations) of Cryptocercus and the sociality

of termites (section 12.4.2) no longer seem likely

Order Blattodea (cockroaches) (see also Box 9.8)

Cockroaches are dorsoventrally flattened insects with

filiform, multisegmented antennae and mandibulate,

ventrally projecting mouthparts The prothorax has an

enlarged, shield-like pronotum, that often covers the

head; the meso- and metathorax are rectangular and

subequal The fore wings are sclerotized tegmina

pro-tecting membranous hind wings folded fan-like beneath

Hind wings often may be reduced or absent, and if

pre-sent characteristically have many vein branches and a

large anal lobe The legs may be spiny and the tarsi are

five-segmented The abdomen has 10 visible segments,

with a subgenital plate (sternum 9), bearing in the male

well-developed asymmetrical genitalia, with one or two

styles, and concealing the reduced 11th segment Cerci

have one or usually many segments; the female

ovipos-itor valves are small, concealed beneath tergum 10

Although long considered an order (and hence

monophyletic) convincing evidence shows the termites

arose from within the cockroaches, and the “order”thus is rendered paraphyletic The sister group of the

Isoptera appears to be Cryptocercus, undoubtedly a

cockroach (Fig 7.4) Other internal relationships of the Blattodea are not well understood, with apparentconflict between morphology and limited moleculardata Usually from five to eight families are recog-nized Blatellidae and Blaberidae (the largest families)are thought to be sister groups The many early fossilsallocated to Blattodea that possess a well-developedovipositor are considered best as belonging to a blattoidstemgroup, that is, from prior to the ordinal diversifica-tion of the Dictyoptera

Order Mantodea (mantids) (see also Box 13.2)

Mantodea are predatory, with males generally smallerthan females The small, triangular head is mobile, withslender antennae, large, widely separated eyes andmandibulate mouthparts The prothorax is narrow and elongate, with the meso- and metathorax shorter.The fore wings form leathery tegmina with a reducedanal area; the hind wings are broad and membranous,with long unbranched veins and many cross-veins, butoften are reduced or absent The fore legs are raptorial,whereas the mid and hind legs are elongate for walk-ing The abdomen has a visible 10th segment, bearingvariably segmented cerci The ovipositor predomin-antly is internal and the external male genitalia areasymmetrical

Mantodea forms the sister group to Blattodea +Isoptera (Fig 7.4), and shares many features withBlattodea such as strong direct flight muscles and weakindirect (longitudinal) flight muscles, asymmetricalmale genitalia and multisegmented cerci Derived features of Mantodea relative to Blattodea involvemodifications associated with predation, including legmorphology, an elongate prothorax, and features asso-ciated with visual predation, namely the mobile headwith large, separated eyes Internal relationships of the eight families of Mantodea are uncertain and littlestudied

Order Grylloblattodea ( = Grylloblattaria, Notoptera) (grylloblattids, ice crawlers or rock crawlers)

(see also Box 9.4)Grylloblattids are moderate-sized, soft-bodied insectswith anteriorly projecting mandibulate mouthpartsand the compound eyes are either reduced or absent.The antennae are multisegmented and the mouthpartsmandibulate The quadrate prothorax is larger than