The Evolution of Wing Dimorphism in Insects
Derek A. Roff
Evolution, Vol. 40, No. 5. (Sep., 1986), pp. 1009-1020.
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Evolutron, 40(5), 1986. pp. 1009-1020
THE EVOLUTION O F WING DIMORPHISM IN INSECTS
DEREK
A. ROFF
McGill University, Department of Biology, 1205 Avenue Dr. PenJield, Montr6a1, Quebec H3A I B I , Canada
Abstract. -Wing-dimorphic insects are excellent subjects for a study of the evolution of dispersal
since the nondispersing brachypterous morph is easily recognized. The purpose of this paper is to
develop a framework within which the evolution ofwing dimorphism can be understood. A review
of the literature indicates that the presence or absence of wings may be controlled by a single locus,
two-allele genetic system or a polygenic system. Both types of inheritance can be subsumed within
a general threshold model.
An increase in the frequency of a brachypterous morph in a population may result from an
increased relative fitness of this morph or the emigration of the macropterous type. The abundance
of wing-polymorphic species argues for an increased fitness of the brachypterous form. An analysis
of the life-history characteristics of 22 species of insects indicates that the brachypterous morph
is both more fecund and reproduces earlier that the macropterous morph. Unfortunately, data on
males are generally lacking.
It is suggested that suppression of wing production results when some hormone, perhaps juvenile
hormone, exceeds a threshold value during a critical stage of development. Further, it is known
that in the monomorphically winged species Oncopeltus fasciatus both flight and oviposition are
regulated by the titer of juvenile hormone. These observations are used to construct a possible
pathway for the evolution of wing dimorphism. This suggests that evolution to a dimorphic species
requires both an increase in the rate of production of the wing suppressing hormone and a change
in the threshold level at which wing and wing-muscle production are suppressed. The stage in this
evolutionary sequence that an organism will reach depends on the stability of the habitat.
Received December 5, 1984. Accepted May 7 , 1986
In a constant environment there may be
circumstances in which dispersal will be a
selectively favorable character (Hamilton
and May, 1977). However, in a spatially and
temporally heterogeneous environment dispersal becomes a virtual necessity, without
which extinction may be very rapid (Roff,
1974a, 19743; Leigh, 1981). The importance of spatial and temporal heterogeneity
in determining population fluctuations and
life-history characteristics has long been
recognized (Elton, 1930; Andrewartha and
Birch, 1953; Southwood, 1962), but it has
been only comparatively recently that detailed theoretical studies have been undertaken. Apart from the not unexpected finding that dispersal can have a strong
stabilizing influence on population fluctuations (Reddingius and den Boer, 1970; Roff,
1974a, 1974b; Vance, 1980; den Boer, 1981;
Kuno, 1981; Hanson and Tuckwell, 198 1;
Hastings, 1982), simulation studies suggest
that dispersal strategies depend upon both
the quantitative and qualitative aspects of
environmental heterogeneity (Van Valen,
1971; Roff, 19743, 1975,1986~;
Palmer and
Strathmann, 1981). The evolution of dispersal strategies will be a function of both
the habitat characteristics and the trade-offs
involved in dispersal. For example, in D.
melanogaster both flight and egg production
depend on the same energy reserves, and
hence dispersal reduces fecundity, with obvious consequences for the fitness of the disperser (Roff, 1977).
A fundamental assumption of any model
or speculation concerning the evolution of
dispersal traits is that these be determined,
at least in part, by the genetic constitution
of the parents of the disperser. This assumption is also of importance with respect
to population dynamics since the numerical
response of a population to changes in environmental parameters depends upon the
mode of inheritance of dispersal tendency
(Roff, 1975). A study of the genetic basis of
dispersal must be able to distinguish between dispersers and nondispersers. In this
regard wing dimorphic insect species are
ideal organisms, since the inability to disperse is clearly recognizable by the absence
of wings (aptery) or wings too small to permit flight (microptery or brachyptery). The
presence of wings does not inevitably mean
that an insect can fly, since in some species
flight muscles may be absent and wings
present (Jackson, 1956a, 19563; Larskn,
1966). Generally, however, this condition
DEREK A. ROFF
morphism? Second, what are the benefits
of being wingless? Finally, what is the likely
evolutionary sequence from a monomorphic winged population to a dimorphic popTHRESHOLD
..-,-.-,-.-,-,-,-,~.~*..-.-~-.-.-.-.--.-.-~-.-.-.-.-.-.-.ulation?
MICROPTEROUS
HORMONE
LEVEL
88
MACROPTEROUS
Bb
bb
GENOTYPE
THRESHOLD
GENOTYPE (HORMONE LEVEL1
FIG.1. A schematic representation of a threshold
model for the determination of pterygomorphism. a)
A single locus, two-allele system in which the brachypterous allele appears dominant because the additive effect of Bb exceeds the threshold level of the
regulatory compound for wing production. b) A polygenic system for wing determination. In both models
the switch from one morph to another is assumed for
convenience to be controlled by the level of a hormone,
although some other substance(s) may be ~nvolved.In
the polygenic model, the level of the hormone can be
equated with the genotype though not with a unlque
genotype.
probably results from the histolysis of the
wing muscles at the onset of reproduction
and after the dispersal episode (Johnson,
1976; Dingle, 1979, 1982). It is relatively
easy to determine whether winged individuals are capable of flight and, hence, whether wing dimorphism is a character by which
a population or family can be divided into
potential dispersers and nondispersers.
Thus. for example, it has been shown that
in Homoptera and Gerridae the degree of
brachyptery is correlated with the stability
of the habitat as is predicted from theoretical considerations (for Homoptera see
Denno, 1978, 1979; Denno et al., 1980;
McCoy and Rey, 198 1; for the Gerridae, see
Vepsalainen, 1973, 1974a, 1978; for a general review see Harrison, 1980).
In this paper, I address three problems.
First, what is the genetic basis of wing di-
The Genetic Basis of Pterygornorphisrn
The simplest model for the genetic determination of pterygomorphism is a single
locus with two alleles, with macroptery being
either dominant or recessive (for convenience I shall refer throughout this discussion to the fully winged condition as
macroptery and the short-winged or wingless conditions as either brachyptery or microptery). At the other extreme the character may be inherited in a polygenic
manner.
Modes of inheritance can be postulated
to be the result of the additive effects of
alleles at a single locus and/or across many
loci. In the case of single-locus inheritance,
either macroptery or brachyptery may appear dominant depending on the values of
the two alleles (Fig. la). A polygenic mode
of inheritance can be understood within the
framework proposed for threshold characters in general (Falconer, 198 1; Roff, 1986b;
Fig. lb).
Of the 22 studies in which it is possible
to suggest a genetic basis for the trait, eight
indicate a simple Mendelian mechanism
(Table 1). I have omitted from Table 1 studies in which environmental factors such as
photoperiod or temperature may be responsible for the observed polymorphism
(Poisson, 1924; Ekblom, 1928, 194 1, 1949)
and those cases in which reduction or loss
of wings is due to a spontaneous mutation
as in Drosophila melanogaster (Eker, 1935),
Pieris napi(Bowden, 1963), or Bombyx mori
(Tazima, 1964).
A polygenic system appears to be the more
general situation, although the number of
loci involved is unknown. It has been shown
that genetic models involving only two or
three loci produce distributions that can only
be distinguished from normal distributions
with very large sample sizes (Thoday and
Thompson, 1976). In general, the sample
sizes from the published analyses on wing
inheritance comprise relatively few families
and individuals (hundreds of individuals
and at best only a dozen or so families).
TABLE1. The probable genetic basis of pterygomorphism in a variety of insect species. Methods of analysis: 1 ) Data from individual crosses; 2) grouped data
from known parent morphs; 3) selection for wing morphs; 4 ) comparison of different geographic strains; 5) comparison of clones.
Order
Family
Species
Mode of inheritance
Coleoptera
Coleoptera
Coleoptera
Coleoptera
Coleoptera
Coleoptera
Coleoptera
Coleoptera
Diptera
Hymenoptera
Hymenoptera
Hemiptera
Curculionidae
Curculionidae
Carabidae
Carabidae
Carabidae
Carabidae
Ptiliidae
Bruchidae
Sphaeroceridae
Bethylidae
Formicidae
Pyrrhocoridae
Sitona hispidula
Apion virens
Pterostichus anthracinus
Bembidion lampros
Calathus erythroderus
Calathus melanocephalus
Ptinella apterae
Callosobruchus maculatus
Apterina pedestris
Cephalonomia gallicola
Harpagoxenus sublaevis
Pyrrhocoris apterous
Single locus, two alleles, brachyptery dominant
Single locus, two alleles, brachyptery dominant
Single locus, two alleles, brachyptery dominant
Single locus, two alleles, macroptery dominant (?)
Single locus, two alleles, brachyptery dominant
Polygenic
Polygenic
Polygenic
Single locus, two alleles, brachyptery dominant
Diploid, apterous; haploid, 2 alleles
Diploid, two alleles, brachyptery dominant
Polygenic
Hemiptera
Gemdae
Gerris lacustris
Polygenic
Hemiptera
Orthoptera
Orthoptera
Orthoptera
Gemdae
Gryllidae
Gryllidae
Gryllidae
Limnoporus caniculatus
Gryllus pennsylvanicus
Gryllus firmus
Gryllodes sigillatus
Polygenic
Polygenic
Polygenic
Polygenic
Orthoptera
Homoptera
Homoptera
Homoptera
Homoptera
Acrididae
Delphacidae
Delphacidae
Delphacidae
Aphididae
Melanoplus lakinus
Laodelphax striatellus
Nilaparvata lugens
Javesella pellucida
Schizaphis gramimum
Insufficient data
Polygenic
Polygenic
Polygenic
Polygenic
Homoptera
Aphididae
Acyrthosiphon pisum
Polygenic
Method
of
analysis
Reference
Jackson, 1928
Stein, 1973a
Lindroth, 1 946b
Langor and Larson, 1 983C
Aukema, unpubl.
Aukema, unpubl.
Taylor, 198 l d
Utida, 1972
Guib6, 1939e
Kearns, 1934
Buschinger, 1978
HonEk 1976a, 19766,
1979
Vepsalainen, 1974b, pers.
c0mm.f
Zera et al., 1983
Hanison, 1979
Roff, 1984, 1986b
Ghouri and McFarlane,
1958
Bland and Nutting, 1969
Mahmud, 1980
Mochida, 1975
Ammar, 1973
Kvenberg and Jones,
1974
Lamb and McKay, 1979
No statisttcal analysts ts presented by S t e m However, it is possible to estimate the expected frequencies from his data; these do not differ significantly from the observed. Given the large number of offspring (855)
the proposed genetlc b a s s can be accepted.
No stat~stlcalanalvs~s
is .resented bv Lindroth. The observed and exwcted frequencies do not differ significantly, but the sample size is small (52 offspring
.
.among
- seven crosses); therefore, any conclusion must
be tentatlve.
Contrary to the contention of Langor and Larsen, a one-locus, two-allele model is consistent with their breeding data. However, the number of offspring from each cross is very low (42 offspring among 16 crosses);
hence the above model serves principally as a basis for further analysis.
~ i t e m a effects
l
could not be discounted.
' N o macropterous ~ndtvtdualshave been found in the wild. However, the presence of well-developed wing muscles In the macropterous individuals (Gu~td.,1939) suggests that the genetlc switch from brachyptery
to macroptery 1s well Integrated wlth the developmental process, and therefore is probably not a spontaneous mutation.
Vepsiila~nen(19746) hypothesized a super gene with a temperature switch. Data on G e m s lacusrris were not entirely consistent with this model (Vepsilainen, 1974b). and in another gerrid, L ~ m n o p o r u scanrculafus.
a polygen~cbasis is evldent (Zera et al., 1983).
a
-
c-.L 0
c-.L
1012
DEREK A. ROFF
tality cost of dispersal might mitigate against
flight but need not in themselves select for
flightlessness since a fully winged individual
need not fly. The evolution of flightlessness
in so large an array of insect orders, families,
and species suggests that there is a cost to
possessing the capability of flight whether
or not flight ever occurs. Table 2 summarizes data on comparisons between life history characteristics in macropterous and
micropterous (including brachypterous or
apterous) morphs of a wide range of insect
species. I have omitted from this table several studies in which the experimental deThe Fitness of the Two Wing Morphs
sign or data base are clearly inadequate (for
For a vestigal or brachypterous mutation Homoptera the study by Watson and Sinha
to spread in a population other than by ge- [I9591 and for gerrids the studies of Poisson
netic drift it must either possess a higher [1924], Brinkhurst [l959], Anderson [1973];
fitness within that population or be pre- see Zera [I9841 for a detailed discussion on
served simply because the winged individ- the genid data). Statistically nonsignificant
uals disperse, leaving the flightless individ- differences between morphs may not be very
uals as an isolated population. The latter informative, since they may arise as a result
circumstance may account for the high fre- of small sample size and/or high variation.
There are no consistent trends in develquency of flightless D. melanogaster found
in a deep pit with decomposing fruit (Du- opment time between macropterous and
binin et al., 1937; cited by Dobzhansky, micropterous morphs; in most instances
195 1 p. 64). Wing polymorphism is com- there are no differences. A similar pattern
mon in the Orthoptera, Hemiptera, Ho- is found for adult longevity, at least for femoptera, Plecoptera, and Coleoptera. In ad- males. There are clear trends in preovipodition, wing reduction in one or both sexes sitional period and fecundity. In the former
is found in most insect orders (for examples case the brachypterous morph either begins
see Kalmus, 1945; Brues et al., 1954; Pois- reproduction before or at the same time as
son, 1946; C.S.I.R.O., 1970; in the subclass the macropterous morph. Brachypterous fePterygota I can find examples of wing re- males consistently produce more eggs than
duction in all orders except the Ephemer- macropterous. Notable exceptions are Ptioptera, Odonata, and Megaloptera). The nella apterae, P. errabunda, and Orgyia
prevalence of wing polymorphism and the thyellina in which the winged morph promore extreme case of complete wing reduc- duces significantly more eggs than the wingtion argues against preservation by isolation less morph (Taylor, 1978; Sato, 1977).
Brachypterous Orgyia thyellina usually
of vestigial-winged individuals as being the
lay diapause eggs, while macropterous fegeneral explanation.
What are the advantages of being flight- males lay nondiapause eggs (Kimura and
less? Flight is energetically expensive (Weis- Masaki, 1977). These eggs differ greatly in
Fogh, 1952; Hocking, 1953; Sotavalta and size, those from the brachypterous females
Laulajainen, 196 1; Yurkiewicz, 1965), and weighing 0.267 mg and from macropterous
in Drosophila species it reduces egg pro- only 0.180 mg (Sato, 1977). Although braduction (Roff, 1977; Inglesfield and Begon, chypterous females lay on average 390.4 eggs
1983). Dispersal may also be risky in that compared to 476.9 eggs laid by macropterit may increase the chance of being preyed ous females, the total reproductive capacity
upon (unfortunately we do not have ade- (egg weight x fecundity) of the latter is
quate estimates of the relative mortality risks greater than the former (104.2 mg compared
of dispersing and non-dispersing insects), to 85.8 mg). If brachypterous females laid
and the disperser may fail to locate a fa- eggs the same size as macropterous females,
vorable habitat. The energy cost and mor- their predicted fecundity would be 579 eggs.
Other studies have involved only mass
crosses of macropterous x macropterous
and brachypterous x brachypterous. For
these reasons, no general conclusion can be
reached on the number of loci involved or
the heritability of the trait. The analysis of
wing inheritance in the cricket Gryllus jrmus (Roff, 1986b) based on over 100 families and 10,000 individuals gives an estimate of heritability of approximately 0.65.
Only further analyses on other species can
establish whether this is a usual value.
1013
WING DIMORPHISM IN INSECTS
TABLE
2. A comparison of life-history parameters between macropterous and brachypterous morphs of various
insect species. 0: no difference between morphs; +: brachypterous morph > macropterous morph; -: brachypterous morph < macropterous morph.
Order
Homoptera Hemiptera Coleoptera Orthoptera
Lepidoptera
Psocoptera
Species
Javesella pellucida
Javesella pellucida
Javesella pellucida
Doratura stylata
Laodelphax striatellus
Stenocranus minutus
Nilaparavata lugens
Nilaparavata lugens
Nilaparavata lugens
Sogata furcifera
Delphacodes striatella
Delphacodes striatella
Sitobion avenae
Metopolophium dirhodum
Aphis fabae
Drepanosiphum dixoni
Macrosiphum granarium
Rhopalosiphum prunifoliae
Aphis maidis
Sigara dorsalis
Sigara fallen;
Sigara scotti
Limnoporus canaliculatus
Ptinella apterae
Ptinella errabunda
Sitona hispidula
Callosobruchus maculatus
Concocephalus discolor
Zonocerus variegatus
Pteronemobius taprobanensis
Pteronemobius nitidus
Gryllodes sigillatus
Gryllus jirrnus
Allonemobius fasciatus
Orgyia thyellina
Graphopsocus cruciatus
Ectopsocus briggsi
Develop- Pre-oviment
positional
time
period
0
0
-
Fecundity
Adult lon-
gevlty
+, Oa
0
0
OC
OC
+c
+C
-b,c
-b,c
OC
-c
-c,d
0
0
0
0
-
+c
0
0
0
0
0
+
+
+
+
+
+
+
+
+
+
-J
-J
-J
of
of
of
-
+g
+g
+
+
+
-
-
-
-
+"
+
+
-c,d
+c
-
-
0
+
Ok
+I
0
Oh
Oh -g
+"
+
+, Oa
-
I
0
0
Reference Ammar, 1973
Mochida, 1973
Waloff, 1973
Waloff, 1973
Mitsuhashi and Koyama,
1974
May, 1975
Nasu, 1969
Manjunath, 1977e
Kisimoto, 1965e
Kisimoto, 1965e
Kisimoto, 1965e
Tsai et a]., 1964
Wratten, 1977
Wratten, 1977
Dixon and Wratten, 1971
Dixon, 1972
Noda, 1960
Noda, 1960
Noda, 1960
Young, 1965
Young, 1965
Young, 1965
Zera, 1984
Taylor, 1978
Taylor, 1978
Jackson, 1928
Caswell, 1960; Utida,
1972
Ando and Hartley, 1982
McCaffery and Page, 1978
Tanaka, 1976
Tanaka, 1978
Ghouri and McFarlane,
1958
Roff, 1984
Roff, 1984
Sato, 1977
New, 1969
New, 1969
a Fecundity of brachypterous morph significantly greater than that of the macropterous In the early stage of reproduction but no signlficant difference
over the total lifespan.
Based on appearance of mature adults in the held and therefore may include differences in development tlme of nymphs.
No statistical analysis and ~nsufficientdata presented to undertake such an analysis. However, the differences between the groups are sufficient
to conclude that a signlficant difference probably exists. Likewise, In those Instances where no difference is indicated, the difference 1s very small.
The delay In reproduction of the macropterous morph is supported by examination of ovariole development.
Unpublished statistical analysis of data presented in paper.
'Analys~s of field populations. Polymorphism is in flight muscles rather than wings, but morphs can be distinguished externally.
g Under conditions of starvation. The method of statistical analysis by Young (1965) 1s incorrect. Insufficient information Bven to perform a correct
test.
No data are presented to support this contention. ' Eggs produced by the brachypterous morph are larger than those of the macropterous (see text). J The difference in development time is in part due to a higher threshold temperature for development in the macropterous form. Arai (1978 Japanese with English summary) states that the macropterous morph takes longer to develop at 35'C than the micropterous. ~npublishehanalysis of larger data set than analyzed in Roff (1984) where "no differences" are reported. *
'
Thus the negative sign in the fecundity column of Table 2 is somewhat misleading.
Despite the exceptional case of Ptinella,
the data strongly suggest that brachypterous
females are more fecund than macropters.
Data for males are generally lacking. Mochida (1973) found no difference in the development of the male reproductive structures
1014
DEREK A. ROFF
of the two wing morphs of Javesella pellucida. Alate males of the hymenopteran Trichogrammatoidea armigera are able to inseminate more females than apterous males
(Manjunath, 1972). But in this species apterous males appear to be developmental
aberrations: these males are almost invariably associated with a female, the two individuals developing from a single fertilized
egg. It is hypothesized "that one of the
cleavage nuclei or polar bodies becomes
separated off along with a little cytoplasm
from the parent cell and develops independently" (Manjunath, 1972 p. 146). In both
male and female macropterous Callosobruchus maculatus the abdominal cavity is filled
by fat body at adult emergence whereas in
the micropterous form both ovaries and
testes are well developed (Utida, 1972). The
relative percentage of micropterous males
differs between species and in some cases,
as with Gryllus firmus (Roff, 1984, 1986b)
there may be a higher frequency of micropterous males than females. This suggests that
being winged carries some cost, even in
males.
The Evolution of Wing Dimorphism
The sequence of events in the average
macropterous insect is:
wing
production
+
wing
muscle
production
-
-
disovipersal position
L, muscle _S
histolysis
with overlap in events, particularly wing and
muscle development.
It has been suggested that brachyptery results when the level of some hormone, possibly juvenile hormone, exceeds a threshold
value during a critical period in development (Southwood, 196 1; Wigglesworth,
196 1). Both flight and oviposition are regulated by the titer of juvenile hormone in
Oncopeltus fasciatus (Rankin, 1978; Rankin and Riddiford, 1978; Slansky, 1980) and
it is likely that the genetic variation in flight
duration (Dingle, 1968, 1980) is actually due
to genetic variation in the rate of production
of juvenile hormone. Polygenic control of
flight duration has also been demonstrated
in Lygaeus kalmii (Caldwell and Hegmann,
1969) and various Cicadulina species (Rose,
1972). Assuming the dispersal syndrome to
be controlled in both its morphological and
behavioral aspects by the titer of juvenile
hormone we can construct a possible evolutionary sequence from monomorphic
macroptery (as in 0.fasciatus) to wing dimorphism as follows (Fig. 2). If genetic variation exists in the amount of flight required
to initiate reproduction, some individuals
with wings and wing muscles will reproduce
without dispersing (Fig. 2a). Differences in
habitat stability will, therefore, select for differences in the readiness to disperse and
amount of flight required to initiate reproduction. Such differences have been found
in different geographic populations of Oncopeltus fasciatus (Dingle, 1978, 1980) and
between species comparisons of Dysdercus
(Dingle and Arora, 1973; Derr et al., 198 1).
As habitat stability increases, selection will
probably favor an increasing proportion of
nondispersers, and the distribution of juvenile hormone will shift as shown in Figure
2b. At this point the population contains
individuals that produce wings but not wing
muscles. These individuals reproduce without dispersing and have a selective advantage over those that do not disperse but still
produce wing muscles, since energy can be
immediately channelled into reproduction.
An increase in the frequency of individuals
that do not produce wing muscles will be
opposed by the decrease in the proportion
of dispersing types produced (Fig. 2b). Selection then favors a change in the threshold
level at which dispersal is initiated, eventually making the thresholds ofwing-muscle
production and dispersal equivalent (Fig.
2c). Such a change may involve a shift in
only one threshold level, as shown in Figure
2c, or a change in both levels to make them
coincident.
Although the production of wings per se
may not be energetically expensive, there
may be selection against wing production
simply as an indirect result of selection for
earlier oogenesis, which requires selection
of those individuals with yet higher rates of
juvenile hormone production and a common threshold for flight capability (Fig. 2d).
Furthermore, there will be selection of modifications that enhance reproduction, such
as an enlargement of body parts concerned
with egg production and a reduction of those
WING DIMORPHISM IN INSECTS
AND DISPERSAL
W ~ N G S WING MUSCLES
INHIBITED
>
A
!
0
Z C
W
3
I
WING
0
(0
W
MUSCLES
AND DISPERSAL INHIBITED
>
>
=Z<
0
3
0 W
a
I
1
DISPERSAL
N H i B T E D
WlNG
MUSCLES
INHIBITED
WINGS
NHlBiTED
HORMONE LEVEL
FIG.2. A possible evolutionary sequence of wing
polymorphism from a macropterous population. Following the sequence from bottom to top: a) The distribution of juvenile hormone (JH) production is such
that all members of the population are macropterous.
However a small percentage have a sufficiently high
production of J H that egg production is initiated without dispersal. b) A higher frequency of nondispersal
being favored, the proportion of individuals producing
high levels of J H increases in the population. The shift
in the distribution produces a small proportion of individuals that abort wing muscle production. The intermediate type (nondisperser with wing muscles) is
selected out of the population by selection of individuals with a threshold level for dispersal that is coincident with the threshold for wing muscle production.
c) A higher frequency of nondispersers can now be
produced without decreasing the proportion of dispersers. The shift in the frequency distribution of J H production produces some individuals that abort wing
production. d) Selection for earlier oogenesis and/or
for structural modifications of the micropterous morph
produces a strictly dimorphic population.
concerned with flight. There is a complete
spectrum of degrees of external modifications, from practically none to radical
changes that make the morphs entirely different in structure (Fig. 3).
Concluding Comments
It seems likely that the flight and reproductive systems are coupled in both males
and females. In winged individuals energy
is channelled into the production and maintenance of the wing muscles, which in many
species are not fully developed at the time
FIG.3. Some examples of micropterous (right side)
and macropterous (left side) morphs showing the variation in differences in morphology between the two
types. The two morphs are drawn to the same scale for
each species except (c), in which the micropterous morph
is eleven-tenths the size of the macropterous morph.
a) Pterostichus anthracinus: no obvious external morphological differences between the morphs (redrawn
from Lindroth, 1946). b) Gelis corruptor: the thorax of
the macropterous morph is more robust than that of
the micropterous (redrawn from Salt, 1952). c) Halticus chrysolepis: Morphological differences between
the two morphs involve the entire body shape (redrawn
from Zimmerman, 1948). d) Plastosciara perniciosa:
the differences in the two morphs are so great that they
might be classified as separate species (redrawn from
Steffan, 1975).
of adult emergence (Williams et al., 1943; Balboni, 1967; De Kort, 1969; Anderson
and Finlayson, 1973; Ready and Josephson,
1982). In micropterous individuals, this en-
1016
DEREK A. ROFF
ergy can be channelled immediately into the
development of the reproductive organs. As
the energetic cost of producing and maintaining the wing muscles is probably much
greater than actually producing the wings
per se the "decision" whether to become
capable of flight may be made after the full
development of the wings. Wings develop
at an earlier stage than flight muscles; thus,
it is not unexpected to find some species in
which all individuals are fully winged but
which are polymorphic with respect to wingmuscle development. It is not clear how
common this phenomenon is, since it requires considerable labor to detect, and the
appropriate studies have been undertaken
for relatively few species (Jackson, 1956a,
1956b; LarsCn, 1966). It is also not clear
how frequently this polymorphism is simply a result of histolysis of the wing muscles
immediately prior to reproduction. There
are also instances in which muscle regeneration may occur (Chapman, 1956; Morgan et al., 1984). There are frequently significant morphological differences between
brachypterous and macropterous morphs,
attaining an extreme form in the dipteran
PIastosciara perniciosa in which the micropterous morph more closely resembles a
maggot than the typical fly-like macropterous morph (Steffan, 1973, 1975). The multiplicity of changes that may accompany the
loss of flight suggests that, in many if not
most cases, the developmental changes that
must occur may well disrupt the production
of wings.
Any fecundity advantage that accrues to
a flightless morph will be offset by the disadvantage of the inability to disperse. If the
habitat is ephemeral and patchy, a polymorphism may be established provided the
winged morph mates prior to dispersal and/
or the trait has a polygenic basis. Mating
prior to dispersal is a necessity for those
species in which macroptery is a recessive
character. The increase in the brachypterous morph of Apion virens and Sitona hispidulus in newly colonized fields (Stein,
1977) suggests that mating does occur prior
to dispersal in these species.
If a habitat is stable for long periods or
distributed so that an insect can move from
one patch to another by walking, hopping
or swimming, the polymorphism will shift
towards the micropterous morph. An extreme result of this shift may be the complete loss of the macropterous morph and
an entirely wingless population or species.
Although habitat stability and/or small interpatch distances are essential for the persistence of a completely flightless morph,
other factors may accelerate or retard the
evolution from polymorphism to monomorphism. For example, life under bark or
d e e ~within leaf litter or caves mav favor
modifications that will lead to loss okwings
(Dybas, 1960; Barr, 1967; Hackman, 1964;
Hamilton, 1978). The coleopteran species
AgIyptinus dimorphicus is particularly interesting as it is found in both caves and
forest litter. The cave populations are all
short-winged whereas the forest litter populations are polymorphic (Peck, 1972). An
increased understanding of the genetic and
physiological basis and evolution of wing
polymorphism may shed considerable light
both on the evolution of dispersal strategies
in general and specifically on the evolution
of monomorphically flightless species, as has
occurred in many insects.
My considerable thanks go to Ms. Janice
Joyce of the McGill Botany-Genetics library for her efficiency and speed at tracking
down and procuring the references cited in
this paper. This study was supported by
NSERC Operating Grant A7764.
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