The Insects - Outline of Entomology 3th Edition - Chapter 5 pot

5.3 SEXUAL SELECTION Many insects are sexually dimorphic, usually with the male adorned with secondary sexual characteristics,some of which have been noted above in relation tocourtship

Two male stick-insects fighting over a female (After Sivinski 1978.)

Chapter 5

REPR ODUCTION

Most insects are sexual and thus mature males and

females must be present at the same time and place for

reproduction to take place As insects are generally

short-lived, their life history, behavior, and

reproduct-ive condition must be synchronized This requires

finely tuned and complex physiological responses to

the external environment Furthermore, reproduction

also depends on monitoring of internal physiological

stimuli, and the neuroendocrine system plays a key

regulatory role Mating and egg production in many

flies is known to be controlled by a series of hormonal

and behavioral changes, yet there is much still to learn

about the control and regulation of insect

reproduc-tion, particularly if compared with our knowledge of

vertebrate reproduction

These complex regulatory systems are highly

suc-cessful For example, look at the rapidity with which

pest insect outbreaks occur A combination of short

generation time, high fecundity, and population

syn-chronization to environmental cues allows many

insect populations to react extremely rapidly under

appropriate environmental conditions, such as a crop

monoculture, or release from a controlling predator

In these situations, temporary or obligatory loss of

males (parthenogenesis) has proved to be another

effective means by which some insects rapidly exploit

temporarily (or seasonally) abundant resources

This chapter examines the different mechanisms

associated with courtship and mating, avoidance of

interspecies mating, ensuring paternity, and

deter-mination of sex of offspring Then we examine the

elim-ination of sex and show some extreme cases in which

the adult stage has been dispensed with altogether

These observations relate to theories concerning sexual

selection, including those linked to why insects have

such remarkable diversity of genitalic structures The

concluding summary of the physiological control of

reproduction emphasizes the extreme complexity and

sophistication of mating and oviposition in insects

5.1 BRINGING THE SEXES TOGETHER

Insects often are at their most conspicuous when

syn-chronizing the time and place for mating The flashing

lights of fireflies, the singing of crickets, and cacophony

of cicadas are spectacular examples However, there is

a wealth of less ostentatious behavior, of equal

signific-ance in bringing the sexes together and signaling

readi-ness to mate to other members of the species All signals

are species-specific, serving to attract members of theopposite sex of the same species, but abuse of these com-munication systems can take place, as when females

of one predatory species of firefly lure males of anotherspecies to their death by emulating the flashing signal

of that species

Swarmingis a characteristic and perhaps mental behavior of insects, as it occurs amongst someinsects from ancient lineages, such as mayflies andodonates, and also in many “higher” insects, such as fliesand butterflies Swarming sites are identified by visualmarkers (Fig 5.1) and are usually species-specific,although mixed-species swarms have been reported,especially in the tropics or subtropics Swarms are pre-dominantly of the male sex only, though female-onlyswarms do occur Swarms are most evident whenmany individuals are involved, such as when midgeswarms are so dense that they have been mistaken forsmoke from burning buildings, but small swarms may

funda-be more significant in evolution A single male insectholding station over a spot is a swarm of one – he awaitsthe arrival of a receptive female that has respondedidentically to visual cues that identify the site The pre-cision of swarm sites allows more effective mate-findingthan searching, particularly when individuals are rare

or dispersed and at low density The formation of aswarm allows insects of differing genotypes to meet andoutbreed This is of particular importance if larvaldevelopment sites are patchy and locally dispersed;inbreeding would occur if adults did not disperse

In addition to aerial aggregations, some male insectsform substrate-based aggregations where they maydefend a territory against conspecific males and/orcourt arriving females Species in which males hold territories that contain no resources (e.g ovipositionsubstrates) important to the females and exhibit male –male aggression plus courtship of females are said tohave a lekmating system Lek behavior is common infruit flies of the families Drosophilidae and Tephritidae.Polyphagous fruit flies should be more likely to have alek mating system than monophagous species because,

in the latter, males can expect to encounter females atthe particular fruit that serves as the oviposition site.Insects that form aerial or substrate-based matingaggregations often do so on hilltops, although someswarming insects aggregate above a water surface oruse landmarks such as bushes or cattle Most speciesprobably use visual cues to locate an aggregation site,except that uphill wind currents may guide insects tohilltops

In other insects, the sexes may meet via attraction to

a common resource and the meeting site might not be

visually located For species whose larval development

medium is discrete, such as rotting fruit, animal dung,

or a specific host plant or vertebrate host, where better

for the sexes to meet and court? The olfactory receptors

by which the female dung fly finds a fresh pile of dung

(the larval development site) can be employed by both

sexes to facilitate meeting

Another odoriferous communication involves one or

both sexes producing and emitting a pheromone,

which is a chemical or mixture of chemicals

percept-ible to another member of the species (section 4.3.2)

Substances emitted with the intention of altering the

sexual behavior of the recipient are termed sex

pheromones Generally, these are produced by the

female and announce her presence and sexual ability to conspecific males Recipient males that detectthe odor plume become aroused and orientate fromdownwind towards the source More and more insectsinvestigated are found to have species-specific sexpheromones, the diversity and specificity of which areimportant in maintaining the reproductive isolation

avail-of a species

When the sexes are in proximity, mating in somespecies takes place with little further ado For example,when a conspecific female arrives at a swarm of maleflies, a nearby male, recognizing her by the particu-lar sound of her wingbeat frequency, immediately copulates with her However, more elaborate and spe-cialized close-range behaviors, termed courtship, arecommonplace

Bringing the sexes together 115

Fig 5.1 Males of the Arctic fly Rhamphomyia nigrita (Diptera: Empididae) hunt for prey in swarms of Aedes mosquitoes (lower

mid-right of drawing) and carry the prey to a specific visual marker of the swarm site (left of drawing) Swarms of both the

empidids and the mosquitoes form near conspicuous landmarks, including refuse heaps or oil drums that are common in parts

of the tundra Within the mating swarm (upper left), a male empidid rises towards a female hovering above, they pair, and theprey is transferred to the female; the mating pair alights (lower far right) and the female feeds as they copulate Females appear toobtain food only via males and, as individual prey items are small, must mate repeatedly to obtain sufficient nutrients to develop abatch of eggs (After Downes 1970)

Box 5.1 Courtship and mating in Mecoptera

Sexual behavior has been well studied in hangingflies

(Bittacidae) of the North American Hylobittacus (Bittacus)

apicalis and Bittacus species and the Australian bittacus species, and in the Mexican Panorpa scor-

Harpo-pionflies (Panorpidae) Adult males hunt for arthropodprey, such as caterpillars, bugs, flies, and katydids.These same food items may be presented to a female

as a nuptial offering to be consumed during copulation.Females are attracted by a sex pheromone emittedfrom one or more eversible vesicles or pouches near theend of the male’s abdomen as he hangs in the foliageusing prehensile fore tarsi

Courting and mating in Mecoptera are exemplified

by the sexual interactions in Harpobittacus australis

(Bittacidae) The female closely approaches the “calling”male; he then ends pheromone emission by retractingthe abdominal vesicles Usually the female probes theprey briefly, presumably testing its quality, while themale touches or rubs her abdomen and seeks her geni-talia with his own If the female rejects the nuptial gift,she refuses to copulate However, if the prey is suitable,the genitalia of the pair couple and the male temporarilywithdraws the prey with his hind legs The female lowersherself until she hangs head downwards, suspended byher terminalia The male then surrenders the nuptialoffering (in the illustration, a caterpillar) to the female,which feeds as copulation proceeds At this stage themale frequently supports the female by holding eitherher legs or the prey that she is feeding on The deriva-tion of the common name “hangingflies” is obvious!Detailed field observations and manipulative experi-ments have demonstrated female choice of male part-ners in species of Bittacidae Both sexes mate severaltimes per day with different partners Females discrimin-ate against males that provide small or unsuitable preyeither by rejection or by copulating only for a short time,which is insufficient to pass the complete ejaculate.Given an acceptable nuptial gift, the duration of copula-tion correlates with the size of the offering Each co-

pulation in field populations of Ha australis lasts from

1 to a maximum of about 17 minutes for prey from 3 to

14 mm long In the larger Hy apicalis, copulations

involving prey of the size of houseflies or larger (19 –

50 mm2) last from 20 to 29 minutes, resulting in maximalsperm transfer, increased oviposition, and the induction

of a refractory period (female non-receptivity to othermales) of several hours Copulations that last less than

20 minutes reduce or eliminate male fertilization cess (Data after Thornhill 1976; Alcock 1979.)

suc-5.2 COURTSHIP

Although the long-range attraction mechanisms

dis-cussed above reduce the number of species present at

a prospective mating site, generally there remains an

excess of potential partners Further discrimination

among species and conspecific individuals usually

takes place Courtship is the close-range, intersexual

behavior that induces sexual receptivity prior to (and

often during) mating and acts as a mechanism for

species recognition During courtship, one or both

sexes seek to facilitate insemination and fertilization by

influencing the other’s behavior

Courtship may include visual displays,

predomin-antly by males, including movements of adorned parts

of the body, such as antennae, eyestalks, and “picture”

wings, and ritualized movements (“dancing”) Tactile

stimulation such as rubbing and stroking often occurs

later in courtship, often immediately prior to mating,

and may continue during copulation Antennae, palps,

head horns, external genitalia, and legs are used in

tactile stimulation

Insects such as crickets, which use long-range

call-ing, may have different calls for use in close-range

courtship Others, such as fruit flies (Drosophila), have

no long-distance call and sing (by wing vibration) only

in close-up courtship In some predatory insects,

including empidid flies and mecopterans, the male

courts a prospective mate by offering a prey item as a

nuptial gift (Fig 5.1; Box 5.1)

If the sequence of display proceeds correctly,

court-ship grades into mating Sometimes the sequence need

not be completed before copulation commences On other

occasions courtship must be prolonged and repeated It

may be unsuccessful if one sex fails to respond or makes

inappropriate responses Generally, members of

differ-ent species differ in some elemdiffer-ents of their courtships

and interspecies matings do not occur The great

spe-cificity and complexity of insect courtship behaviors can

be interpreted in terms of mate location, synchronization,

and species recognition, and viewed as having evolved

as a premating isolating mechanism Important as this

view is, there is equally compelling evidence that

court-ship is an extension of a wider phenomenon of

competit-ive communication and involves sexual selection

5.3 SEXUAL SELECTION

Many insects are sexually dimorphic, usually with the

male adorned with secondary sexual characteristics,some of which have been noted above in relation tocourtship display In many insect mating systemscourtship can be viewed as intraspecific competition formates, with certain male behaviors inducing femaleresponse in ways that can increase the mating success

of particular males Because females differ in theirresponsiveness to male stimuli, females can be said

to choose between mates, and courtship thus is petitive Female choice might involve no more thanselection of the winners of male–male interactions,

com-or may be as subtle as discrimination between thesperm of different males (section 5.7) All elements ofcommunication associated with gaining fertilization ofthe female, from long-distance sexual calling through

to insemination, are seen as competitive courtshipbetween males By this reasoning, members of a speciesavoid hybrid matings because of a specific-mate recog-nition system that evolved under the direction of femalechoice, rather than as a mechanism to promote speciescohesion

Understanding sexual dimorphism in insects such

as staghorn beetles, song in orthopterans and cicadas,and wing color in butterflies and odonates helpedDarwin to recognize the operation of sexual selection – the elaboration of features associated with sexualcompetition rather than directly with survival SinceDarwin’s day, studies of sexual selection often have featured insects because of their short generation time,facility of manipulation in the laboratory, and relativeease of observation in the field For example, dung beetles belonging to the large and diverse genus

Onthophagus may display elaborate horns that vary in

size between individuals and in position on the bodybetween species Large horns are restricted nearlyexclusively to males, with only one species known inwhich the female has better developed protuberancesthan conspecific males Studies show that females preferentially select males with larger horns as mates.Males size each other up and may fight, but there is

no lek Benefits to the female come from long-hornedmales’ better defensive capabilities against intrudersseeking to oust the resident from the resource-rich nestsite, provisioned with dung, his mate, and their young(Fig 9.5) However, the system is more complicated, at

least in the North American Onthophagus taurus In this

dung beetle, male horn size is dimorphic, with insectsgreater than a certain threshold size having largehorns, and those below a certain size having only min-imal horns (Fig 5.2) However, nimble small-horned

males attain some mating success through sneakily

circumventing the large-horned but clumsy male

defending the tunnel entrance, either by evasion or by

digging a side tunnel to access the female

Darwin could not understand why the size and

loca-tion of horns varied, but now elegant comparative

studies have shown that elaboration of large horns

bears a developmental cost Organs located close to a

large horn are diminished in size – evidently resources

are reallocated during development so that either eyes,

antennae, or wings apparently “pay for” being close to

a male’s large horn Regular-sized adjacent organs are

developed in females of the same species with smaller

horns and male conspecifics with weakly developed

horns Exceptionally, the species with the female having

long horns on the head and thorax commensurately

has reduced adjacent organs, and a sex reversal in

defensive roles is assumed to have taken place The

dif-ferent locations of the horns appear to be explained

by selective sacrifice of adjacent organs according to

species behavior Thus, nocturnal species that require

good eyes have their horns located elsewhere than the

head; those requiring flight to locate dispersed dung

have horns on the head where they interfere with eye

or antennal size, but do not compromise the wings

Presumably, the upper limit to horn elaboration either

is the burden of ever-increasing deleterious effects on

adjacent vital functions, or an upper limit on the

vol-ume of new cuticle that can develop sub-epidermally in

the pharate pupa within the final-instar larva, underjuvenile hormonal control

Size alone may be important in female choice: insome stick-insects (also called walking sticks) largermales often monopolize females Males fight over theirfemales by boxing at each other with their legs whilegrasping the female’s abdomen with their claspers (as

shown for Diapheromera veliei in the vignette for this

chapter) Ornaments used in male-to-male combat

include the extraordinary “antlers” of Phytalmia

(Tephritidae) (Fig 5.3) and the eyestalks of a few otherflies (such as Diopsidae), which are used in competitionfor access to the oviposition site visited by females.Furthermore, in studied species of diopsid (stalk-eyedflies), female mate choice is based on eyestalk length up

to a dimension of eye separation that can surpass the body length Cases such as these provide evidencefor two apparently alternative but likely non-exclusiveexplanations for male adornments: sexy sons or goodgenes If the female choice commences arbitrarily forany particular adornment, their selection alone willdrive the increased frequency and development of theelaboration in male offspring in ensuing generations(the sexy sons) despite countervailing selection againstconventional unfitness Alternatively, females maychoose mates that can demonstrate their fitness by carrying around apparently deleterious elaborationsthereby indicating a superior genetic background(good genes) Darwin’s interpretation of the enigma offemale choice certainly is substantiated, not least bystudies of insects

5.4 COPULATION

The evolution of male external genitalia made it sible for insects to transfer sperm directly from male tofemale during copulation All but the most primitiveinsects were freed from reliance on indirect methods,such as the male depositing a spermatophore(spermpacket) for the female to pick up from the substrate,

pos-as in Collembola, Diplura, and apterygote insects Inpterygote insects, copulation (sometimes referred to asmating) involves the physical apposition of male andfemale genitalia, usually followed by insemination –the transfer of sperm via the insertion of part of themale’s aedeagus(edeagus), the penis, into the repro-ductive tract of the female In males of many species theextrusion of the aedeagus during copulation is a two-stage process The complete aedeagus is extended from

Fig 5.2 Relationship between length of horn and body

size (thorax width) of male scarabs of Onthophagus taurus.

(After Moczek & Emlen 2000; with beetle heads drawn by

S.L Thrasher.)

the abdomen, then the intromittent organ is everted

or extended to produce an expanded, often elongate

structure (variably called the endophallus, flagellum,

or vesica) capable of depositing semen deep within the

female’s reproductive tract (Fig 5.4) In many insects

the male terminalia have specially modified claspers,

which lock with specific parts of the female terminalia

to maintain the connection of their genitalia during

sperm transfer

This mechanistic definition of copulation ignores the

sensory stimulation that is a vital part of the copulatory

act in insects, as it is in other animals In over a third of

all insect species surveyed, the male indulges in

copulat-ory courtship – behavior that appears to stimulate thefemale during mating The male may stroke, tap, or bitethe body or legs of the female, wave antennae, producesounds, or thrust or vibrate parts of his genitalia.Sperm are received by the female insect in a copulatory pouch (genital chamber, vagina, or bursacopulatrix) or directly into a spermatheca or its duct (as

in Oncopeltus; Fig 5.4) A spermatophore is the means

of sperm transfer in most orders of insects; only someHeteroptera, Coleoptera, Diptera, and Hymenopteradeposit unpackaged sperm Sperm transfer requireslubrication, obtained from the seminal fluids, and, ininsects that use a spermatophore, packaging of sperm

Fig 5.3 Two males of Phytalmia mouldsi (Diptera: Tephritidae) fighting over access to the oviposition site at the larval substrate

visited by females These tropical rainforest flies thus have a resource-defense mating system (After Dodson 1989, 1997.)

Secretions of the male accessory glands serve both of

these functions as well as sometimes facilitating the

final maturation of sperm, supplying energy for sperm

maintenance, regulating female physiology and, in a

few species, providing nourishment to the female

(Box 5.2) The male accessory secretions may elicit one

or two major responses in the female – induction ofoviposition (egg-laying) and/or repression of sexualreceptivity – by entering the female hemolymph andacting on her nervous and/or endocrine system

Fig 5.4 Posterior ends of a pair of copulating milkweed bugs, Oncopeltus fasciatus (Hemiptera: Lygaeidae) Mating commences

with the pair facing in the same direction, then the male rotates his eighth abdominal segment (90°) and genital capsule (180°),erects the aedeagus and gains entry to the female’s genital chamber, before he swings around to face in the opposite direction The bugs may copulate for several hours, during which they walk around with the female leading and the male walking

backwards (a) Lateral view of the terminal segments, showing the valves of the female’s ovipositor in the male genital chamber;(b) longitudinal section showing internal structures of the reproductive system, with the tip of the male’s aedeagus in the female’sspermatheca (After Bonhag & Wick 1953.)

Sexual selection 121

Box 5.2 Nuptial feeding and other “gifts”

Feeding of the female by the male before, during, or

after copulation has evolved independently in several

different insect groups From the female’s perspective,

feeding takes one of three forms:

1 receipt of nourishment from food collected,

cap-tured, or regurgitated by the male (Box 5.1); or

2 obtaining nourishment from a glandular product

(including the spermatophore) of the male; or

3 by cannibalization of males during or after copulation.

From the male’s perspective, nuptial feeding mayrepresent parental investment (provided that the male

can be sure of his paternity), as it may increase the

number or survival of the male’s offspring indirectly via

nutritional benefits to the female Alternatively,

court-ship feeding may increase the male’s fertilization

suc-cess by preventing the female from interfering with

sperm transfer These two hypotheses concerning the

function of nuptial feeding are not necessarily mutually

exclusive; their explanatory value appears to vary

between insect groups and may depend, at least partly,

on the nutritional status of the female at the time of

mating Studies of mating in Mecoptera, Orthoptera,

and Mantodea exemplify the three nuptial feeding types

seen in insects, and continuing research on these

groups addresses the relative importance of the two

main competing hypotheses that seek to explain the

selective advantage of such feeding

In some other insect orders, such as the Lepidopteraand Coleoptera, the female sometimes acquires meta-bolically essential substances or defensive chemicalsfrom the male during copulation, but oral uptake by thefemale usually does not occur The chemicals are trans-ferred by the male with his ejaculate Such nuptial giftsmay function solely as a form of parental investment (as in puddling; see below) but may also be a form ofmating effort (Box 14.3)

Puddling and sodium gifts in Lepidoptera

Male butterflies and moths frequently drink at pools

of liquid, a behavior known as puddling Anyone who

has visited a tropical rainforest will have seen drinkingclusters of perhaps hundreds of newly eclosed malebutterflies, attracted particularly to urine, feces, andhuman sweat (see Plate 2.6, facing p 14) It has longbeen suggested that puddling – in which copious quant-ities of liquid are ingested orally and expelled anally – results in uptake of minerals, such as sodium, whichare deficient in the larval (caterpillar) folivore diet Thesex bias in puddling occurs because the male uses thesodium obtained by puddling as a nuptial gift for his

mate In the moth Gluphisia septentrionis

(Notodon-tidae) the sodium gift amounts to more than half of thepuddler’s total body sodium and appears to be trans-ferred to the female via his spermatophore (Smedley &

Eisner 1996) The female then apportions much of

this sodium to her eggs, which contain several times

more sodium than eggs sired by males that have been

experimentally prevented from puddling Such paternal

investment in the offspring is of obvious advantage to

them in supplying an ion important to body function

In some other lepidopteran species, such “salted”

gifts may function to increase the male’s reproductive

fitness not only by improving the quality of his offspring

but also by increasing the total number of eggs that he

can fertilize, assuming that he remates In the skipper

butterfly, Thymelicus lineola (Hesperiidae), females

usually mate only once and male-donated sodium

appears essential for both their fecundity and longevity

(Pivnick & McNeil 1987) These skipper males mate

many times and can produce spermatophores without

access to sodium from puddling but, after their first

mating, they father fewer viable eggs compared with

remating males that have been allowed to puddle This

raises the question of whether females, which should

be selective in the choice of their sole partner, can

dis-criminate between males based on their sodium load If

they can, then sexual selection via female choice also

may have selected for male puddling

In other studies, copulating male lepidopterans havebeen shown to donate a diversity of nutrients, includ-

ing zinc, phosphorus, lipids, and amino acids, to their

partners Thus, paternal contribution of chemicals to

offspring may be widespread within the Lepidoptera

Mating in katydids (Orthoptera: Tettigoniidae)

During copulation the males of many species of

katy-dids transfer elaborate spermatophores, which are

attached externally to the female’s genitalia (see Plate

3.1) Each spermatophore consists of a large,

proteina-ceous, sperm-free portion, the spermatophylax, which

is eaten by the female after mating, and a sperm

ampulla, eaten after the spermatophylax has been

consumed and the sperm have been transferred to the

female The illustration (p 121) shows a recently mated

female Mormon cricket, Anabrus simplex, with a

sper-matophore attached to her gonopore; in the

illustra-tion on the upper right, the female is consuming the

spermatophylax of the spermatophore (after Gwynne

1981) The schematic illustration underneath depicts

the posterior of a female Mormon cricket showing the

two parts of the spermatophore: the spermatophylax

(cross-hatched) and the sperm ampulla (stippled) (after

Gwynne 1990) During consumption of the

spermato-phylax, sperm are transferred from the ampulla along

with substances that “turn off ” female receptivity to

fur-ther males Insemination also stimulates oviposition by

the female, thereby increasing the probability that the

male supplying the spermatophore will fertilize the eggs

There are two main hypotheses for the adaptive

significance of this form of nuptial feeding The matophylax may serve as a sperm-protection device bypreventing the ampulla from being removed until afterthe complete ejaculate has been transferred Alternat-ively, the spermatophylax may be a form of parentalinvestment in which nutrients from the male increasethe number or size of the eggs sired by that male Ofcourse, the spermatophylax may serve both of thesepurposes, and there is evidence from different species

sper-to support each hypothesis Experimental alteration

of the size of the spermatophylax has demonstratedthat females take longer to eat larger ones, but in somekatydid species the spermatophylax is larger than isneeded to allow complete insemination and, in thiscase, the nutritional bonus to the female benefits themale’s offspring The function of the spermatophylaxapparently varies between genera, although phylogen-etic analysis suggests that the ancestral conditionwithin the Tettigoniidae was to possess a small sper-matophylax that protected the ejaculate

Cannibalistic mating in mantids (Mantodea)

The sex life of mantids is the subject of some versy, partly as a consequence of behavioral observa-tions made under unnatural conditions in the laboratory.For example, there are many reports of the male beingeaten by the generally larger female before, during, orafter mating Males decapitated by females are evenknown to copulate more vigorously because of the loss

contro-of the suboesophageal ganglion that normally inhibitscopulatory movements Sexual cannibalism has beenattributed to food deprivation in confinement but femalemantids of at least some species may indeed eat theirpartners in the wild

Courtship displays may be complex or absent,depending on species, but generally the female attractsthe male via sex pheromones and visual cues Typically,the male approaches the female cautiously, arrestingmovement if she turns her head towards him, and then

he leaps onto her back from beyond her strike reach.Once mounted, he crouches to elude his partner’sgrasp Copulation usually lasts at least half an hour andmay continue for several hours, during which sperm aretransferred from the male to the female in a sper-matophore After mating, the male retreats hastily If themale were in no danger of becoming the female’s meal,his distinctive behavior in the presence of the femalewould be inexplicable Furthermore, suggestions ofgains in reproductive fitness of the male via indirectnutritional benefits to his offspring are negated by theobvious unwillingness of the male to participate in theultimate nuptial sacrifice – his own life!

Whereas there is no evidence yet for an increase inmale reproductive success as a result of sexual canni-balism, females that obtain an extra meal by eating their

5.5 DIVERSITY IN GENITALIC

MORPHOLOGY

The components of the terminalia of insects are very

diverse in structure and frequently exhibit

species-specific morphology (Fig 5.5), even in otherwise

similar species Variations in external features of the

male genitalia often allow differentiation of species,

whereas external structures in the female usually are

simpler and less varied Conversely, the internal

geni-talia of female insects often show greater diagnostic

variability than the internal structures of the males

However, recent development of techniques to evert

the endophallus of the male aedeagus allows increasing

demonstration of the species-specific shapes of these

male internal structures In general, external genitalia

of both sexes are much more sclerotized than the

inter-nal genitalia, although parts of the reproductive tract

are lined with cuticle Increasingly, characteristics

of insect internal genitalia and even soft tissues are

recognized as allowing species delineation and

provid-ing evidence of phylogenetic relationships

Observations that genitalia frequently are complex

and species-specific in form, sometimes appearing tocorrespond tightly between the sexes, led to formula-tion of the “lock-and-key” hypothesis as an explanation

of this phenomenon Species-specific male genitalia(the “keys”) were believed to fit only the conspecificfemale genitalia (the “locks”), thus preventing inter-specific mating or fertilization For example, in somekatydids interspecific copulations are unsuccessful intransmitting spermatophores because the specificstructure of the male claspers (modified cerci) fails to fitthe subgenital plate of the “wrong” female The lock-and-key hypothesis was postulated first in 1844 andhas been the subject of controversy ever since In many(but not all) insects, mechanical exclusion of “incor-rect” male genitalia by the female is seen as unlikely forseveral reasons:

1 morphological correlation between conspecific male

and female parts may be poor;

2 interspecific, intergeneric, and even interfamilial

hybrids can be induced;

3 amputation experiments have demonstrated that

male insects do not need all parts of the genitalia toinseminate conspecific females successfully

Diversity in genitalic morphology 123

mate may gain a selective advantage, especially if food

is limiting This hypothesis is supported by experiments

with captive females of the Asian mantid Hierodula

membranacea that were fed different quantities of food.

The frequency of sexual cannibalism was higher for

females of poorer nutritional condition and, among the

females on the poorest diet, those that ate their mates

produced significantly larger oothecae (egg packages)and hence more offspring The cannibalized maleswould be making a parental investment only if theirsperm fertilize the eggs that they have nourished Thecrucial data on sperm competition in mantids are notavailable and so currently the advantages of this form ofnuptial feeding are attributed entirely to the female

Fig 5.5 Species-specificity in part of the male genitalia of three sibling species of Drosophila (Diptera: Drosophilidae)

The epandrial processes of tergite 9 in: (a) D mauritiana; (b) D simulans; (c) D melanogaster (After Coyne 1983.)

Some support for the lock-and-key hypothesis comes

from studies of certain noctuid moths in which

struc-tural correspondence in the internal genitalia of the

male and female is thought to indicate their function as

a postcopulatory but prezygotic isolating mechanism

Laboratory experiments involving interspecific

mat-ings support a lock-and-key function for the internal

structures of other noctuid moths Interspecific

copula-tion can occur, although without a precise fit of the

male’s vesica (the flexible tube everted from the

aedea-gus during insemination) into the female’s bursa

(genital pouch); the sperm may be discharged from

the spermatophore to the cavity of the bursa, instead of

into the duct that leads to the spermatheca, resulting

in fertilization failure In conspecific pairings, the

sper-matophore is positioned so that its opening lies opposite

that of the duct (Fig 5.6)

In species of Japanese ground beetle of the genus

Carabus (subgenus Ohomopterus) (Carabidae), the male’s

copulatory piece (a part of the endophallus) is a precise

fit for the vaginal appendix of the conspecific female

During copulation, the male everts his endophallus in

the female’s vagina and the copulatory piece is inserted

into the vaginal appendix Closely related parapatric

species are of similar size and external appearance but

their copulatory piece and vaginal appendix are verydifferent in shape Although hybrids occur in areas ofoverlap of species, matings between different species ofbeetles have been observed to result in broken copulat-ory pieces and ruptured vaginal membranes, as well asreduced fertilization rates compared with conspecificpairings Thus, the genital lock-and-key appears toselect strongly against hybrid matings

Mechanical reproductive isolation is not the onlyavailable explanation of species-specific genital mor-phology Five other hypotheses have been advanced:pleiotropy, genitalic recognition, female choice, inter-sexual conflict, and male–male competition The firsttwo of these are further attempts to account for repro-ductive isolation of different species, whereas the lastthree are concerned with sexual selection, a topic that

is addressed in more detail in sections 5.3 and 5.7.The pleiotropy hypothesis explains genitalic differ-ences between species as chance effects of genes thatprimarily code for other vital characteristics of theorganism This idea fails to explain why genitaliashould be more affected than other parts of the body.Nor can pleiotropy explain genital morphology ingroups (such as the Odonata) in which organs otherthan the primary male genitalia have an intromittent

Fig 5.6 Spermatophores lying within the bursae of the female reproductive tracts of moth species from four different genera(Lepidoptera: Noctuidae) The sperm leave via the narrow end of each spermatophore, which has been deposited so that itsopening lies opposite the “seminal duct” leading to the spermatheca (not drawn) The bursa on the far right contains twospermatophores, indicating that the female has remated (After Williams 1941; Eberhard 1985.)

function (like those on the anterior abdomen in

odon-ates) Such secondary genitalia consistently become

subject to the postulated pleiotropic effects whereas

the primary genitalia do not, a result inexplicable by

the pleiotropy hypothesis

The hypothesis of genitalic recognition involves

reproductive isolation of species via female sensory

discrimination between different males based upon

genitalic structures, both internal and external The

female thus responds only to the appropriate genital

stimulation of a conspecific male and never to that of

any male of another species

In contrast, the female-choice hypothesis involves

female sexual discrimination amongst conspecific

males based on qualities that can vary intraspecifically

and for which the female shows preference This idea

has nothing to do with the origin of reproductive

isola-tion, although female choice may lead to reproductive

isolation or speciation as a by-product The

female-choice hypothesis predicts diverse genitalic logy in taxa with promiscuous females and uniformgenitalia in strictly monogamous taxa This predictionseems to be fulfilled in some insects For example, in

morpho-neotropical butterflies of the genus Heliconius, species

in which females mate more than once are more likely

to have species-specific male genitalia than species inwhich females mate only once The greatest reduction inexternal genitalia (to near absence) occurs in termites,which, as might be predicted, form monogamous pairs.Variation in genitalic and other body morphologyalso may result from intersexual conflict over control

of fertilization According to this hypothesis, femalesevolve barriers to successful fertilization in order tocontrol mate choice, whereas males evolve mech-anisms to overcome these barriers For example, inmany species of water-striders (Gerridae) males possesscomplex genital processes and modified appendages(Fig 5.7) for grasping females, which in turn exhibit

Diversity in genitalic morphology 125

Fig 5.7 Males of three species of the water-strider genus Rheumatobates, showing species-specific antennal and leg modifications

(mostly flexible setae) These non-genitalic male structures are specialized for contact with the female during mating, when

the male rides on her back Females of all species have a similar body form (a) R trulliger; (b) R rileyi; (c) R bergrothi

(After Hungerford 1954.)

Box 5.3 Sperm precedence