Heredity 57 (1986) 221—231 The Genetical Society of Great Britain Received 4 December 1985
The genetic basis of wing dimorphism in the sand cricket, Gryllus firmus and its relevance to the evolution of wing dimorphisms in insects
Derek A. Roff McGill University, Department of Biology, 1205 Avenue Docteur Penfield, Montreal, Quebec, H3A 1B1.
The sand cricket, Gryllus firmus is dimorphic with respect to wing length, some individuals being micropterous and others macropterous. The trait has a polygenic basis, micropterous parents producing a higher proportion of micropterous offspring than macropterous parents. The heritability of the trait, determined under a fixed photoperiod/temperature regime is 062 O•075 and 0•68 0•085 for males and females respectively. An alternate method of determining heritability based on a modified mid-parent on mean offspring regression is presented. This method is predicted to give an underestimate of heritability but permits an analysis of the separate influences of each parent. This analysis indicates the heritability in males and females to be 055 and that there are no maternal effects under the particular rearing conditions. A 5 hour shift in the photoperiod appears not to drastically change the heritability but a change in rearing temperature from 30°C to 25°C probably reduces it. Field observations suggest that at certain times of the year heritability may be relatively high whereas at others it could be very low. The adaptive significance of wing polymorphism and its evolution is discussed.
INTRODUCTION the stability of the habitat, the benefits such as increased fecundity of being flightless and the Withrelatively few exceptions the environment of genetic basis of the trait. living organisms is spatially and temporally The genetic basis of wing dimorphism in insects heterogeneous and hence there must be a continual is not well understood. Studies on a wide variety movement of propagules to colonise empty habi- of insects suggest that although it may in some tats and counterbalance the inevitable local extinc- cases be inherited as a simple mendelian character tions (Andrewartha and Birch, 1954; Southwood, in others it is polygenic (Harrison, 1980; RofI, 1962). The relative ease with which pterygote 1986a). In the latter cases the data are compara- insects can be classified as potential dispersers or tively scanty and insufficient to determine the non dispersers by the presence or absence of func- heritability of the trait. Both single locus and poiy- tional wings make them ideal models for an genic systems can be analyzed within the examination of this phenomenon. framework of "threshold characters". It is assumed In the four large orders of pterygote insects, that loci, or in the case of the single locus system, the Orthoptera, Homoptera, Hemiptera and alleles, interact with their combined effect deter- Coleoptera wing dimorphism is common. The most mining the level of some wing suppressing sub- likely general explanation for the evolution and stance, possibly juvenile hormone (Harrison, 1980; maintenance of such dimorphisms is that although Roff, 1986a). Above a certain level of this sub- wings permit dispersal over relatively long dis- stance wing development is suppressed and tances and hence persistence in a heterogeneous microptery results. Because the character can only environment, the possession of wings and not be scored as "present" or "absent" the usual simply flight carries a fitness "cost" (Roff, 1984; method of genetic analysis, such as parent- 1986a). This cost in females appears, in general, offspring regression, cannot be used. The analysis to be a reduced fecundity and a delay in the start of the inheritance of all or none characters is of oviposition of the winged morph (Dingle, 1980; reasonably well worked out (Dempster and Lerner, Harrison 1980; Roll, 1986a). The frequency of the 1950; Robertson, 1951; Falconer, 1981; Bull, Vogt two wing morphs in a population will depend upon and Bulmer, 1982) but requires that large numbers 222 D. A. ROFF of organisms be raised to ascertain within and 19cm Wx 13 cm H from Fisher Scientific) with a between family variation in the trait. mesh covered hole (approx. 1 cm diameter) along The sand cricket, Gryllusfirmus is well suited the top of each side to provide ventilation. Wooden for an analysis of the heritability of wing dimorph- lids were tried but found to be unsatisfactory due ism: it is easy to rear, easy to score with respect to warping; glass lids proved very satisfactory. to wing length (Macropterous, long, and Water was provided for the early and middle Micropterous, short) and is polymorphic under instars by a cheesecloth wick which passed through natural conditions (Veazey et a!., 1976). The long a hole in the floor of the cage to a reservoir of term goal of this research is to develop a genetic water supplied by sitting the rearing cage in model that will permit a realistic and testable another cage containing water: plastic protruber- examination of the interaction between environ- ances on the sides of the cages kept the rearing mental stability and wing polymorphism in G. cage above the water level of the reservoir cage. firmus. In this paper I report on experiments desig- For the final instars water was supplied from glass ned to estimate the heritability of wing length vials plugged with cotton wool. All cages received under several environmental conditions. either lettuce and Purina© cat chow, ad libitum and crushed to provide a range in food particle size, or cat chow and Purina© rabbit chow similarly MATERIALS AND METHODS crushed. Although development time varied on these two diets the proportion macroptery did not differ significantly and the data have been com- Species description and rearing method bined for the present analysis. Gryllus firmus is a large (adult weight approxi- mately 07 gms) ground dwelling cricket occurring in the southeastern United States (Alexander, ExperimentalDesign 1968). It is closely related to other Gryllus species Theexperimental design is outlined schematically and recent electrophoretic evidence suggests that in fig. 1. To avoid, as much as possible, environ- it may be distributed further north than hitherto mental influences via maternal effects an initial supposed and may hybridise with Gryllus pennsyl- parental generation was established at the tem- vanicus (Harrison and Arnold, 1982). In addition, perature and photoperiod under which subsequent Gryllus bermudensis from the Bermudas is now generations were raised. Heritability of a threshold considered a subspecies of G.firmus (Kevan, 1980) trait is determined most precisely when the propor- indicating that this species has a wide distribution. tion in each category is close to half, the variance Its typical habitat is flat sandy areas both inland in the estimated value being smallest at this value. and bordering ocean beaches (Harrison, 1979). I therefore, selected a photoperiod and tem- The specimens used in the present study are perature accordingly: the selected regime was derived from approximately forty individuals (approximately 20 females) captured at a single locale in northern Florida. Alexander (1968) indi- cates that G. firmus is univoltine with an egg diapause and spring and fall populations. The presence of spring and fall populations produces two population peaks and the appearance of a bivoltine cycle (Veazey et aL, 1976). However, diapause is not obligatory for all eggs and thus the two populations are not entirely separate (Walker, 1980). The stock used in the present analysis has been maintained continuously for three years (approximately 15 generations) with no signs of decreased fertility or vitality. This stock is maintained at approximately 100-300 breeding individuals at a temperature of 25-30°C. Heat is provided by two 100 watt electric light bulbs oper- F3 GENERATION ated thermostatically; hence there is no set photo INTRA-FAMILY CROSSES period. For the breeding experiments the crickets were raised in disposable mouse cages (29 cm Lx Figure 1Schematic illustration of experimental design. WING DIMORPHISM IN A SAND CRICKET 223 17 hrs L: 7 hrs D at 30°C which produced an the genetic basis of the trait is to examine the average proportion of macropterous females and proportion of macropterous offspring in relation males in the combined F1 and F2 generations of to the parental morphs. We expect that if the trait 0758 and 0638 respectively. has a genetic basis the proportion of macropterous There is generally no difficulty in differentiating offspring from macropterous parents will be macropterous and micropterous morphs: in the greater than that from micropterous parents. If the latter the wings are very small and fully hidden by trait is polygenic there will nevertheless be a con- the tegmina. Occasionally an individual had hind tinuous distribution of percentage macroptery in wings that protruded beyond the tegmina but were the offspring from a given type of parental cross. not as long as in the macropterous morph. Of 8574 Having demonstrated that there is a genetical basis individuals raised in the F1 and F2 generations to the trait and that it is polygenic we proceed to only 125 per cent (107) had such intermediate estimate the additive component, the heritability. wings. These were discarded from the analysis. The general statistical background for the esti- In generations F1 and F2 all parents for each mation of heritability from family data is outlined cross came from different families. In the F3 gener- in Dempster and Lerner (1950) and Bull et a!. ation intra-family crosses were made. In general (1982). The first step is to compute the intraclass each cross comprised two cages, each started with correlation coefficient. Three separate methods are 60 newly emerged nymphs, the offspring from a available which I shall call the Anova method single pair mating. Survival averaged 63 per cent (Elston, 1977), the Maximum Likelihood method giving approximately 76 individuals per family, and the x2method.The rationales underlying the which gives a reasonably precise estimate of the latter two are described by Robertson (1951). proportion macropterous. Much of the mortality Using the Anova method the intraclass correlation, appears to be due to cannabalism by the males r, is computed as which are very aggressive. There is no indication of selective mortality of the different morphs, the (MSA— MS) correlation between per cent survival and per cent T(MS+(kl)MS) female macropterous offspring being insignificant where MSA is the mean square among families, (r=—0.14, n=110, P>010, arcsine trans- MS is the mean square within families and k is formation). Each cage was inspected twice weekly equal to (N_:c1 n/N)/(C—1), where n, is the for adults or more frequently as labour permitted. number of individuals in family i, C is the number Cages in the parental generation were inspected of families and N is the total number of individuals daily, except on weekends. (N = Environmental factors may alter the proportion n1). The MSA and MS are estimated by of macropterous individuals produced. To examine the influence of one such factor, photo- MSA= m/n1—( m1)2/N period, on the genetic expression of the trait, 14 (C-i) families were divided into two groups, one reared m— m/n, at a photoperiod of 17 L: 7 D and the other at 12 L: MS- 12 D. Temperature is also known to influence the (N-C) expression of the trait. No experiments on the where rnis the number of macropterous effect of temperature using the split family design individuals in family i and the summation is taken have yet been undertaken but data are reported from i =1to i =C. on an experiment in which offspring from a mixture Using the x2methodr is computed from the of parents were raised at 30°C and 25°C. expression. r=(2—(C —1)) Statisticalanalysis C Rearingmembers of the same family in two separ- ate cages permits a preliminary examination of the where x2is genetical basis of the trait. If there is a genetic ,2j rn/n—( rn1)2/N component to macroptery the proportion of p(i—p) macropterous individuals in each cage should be similar. This can be statistically tested with the and p is the mean proportion of macropterous intraclass correlation coefficient (Snedecor and individuals per family (p =(1/C)(rn/n),see Cochran, 1967). A second method of establishing Bull et a!., 1982). 224 D. A. ROFF The Maximum Likelihood method, unlike the bilitthat an individual is macropterous is given — previous two assumes a constant family size. by J Q(x —p.s)dx. Letting y =xp.,the preced- However, because of its efficiency Robertson ing expression becomes $ Q(y) dy. The value of (1951) recommends this method above the x2 p., is the ordinate on the standardised normal curve method when the variability in n is large. The which corresponds to p,the proportion of macrop- approximate maximum likelihood estimate of r is terous individuals in family i. This value can be obtained from the tables in Finney (1971) or from 2p(1—p)K1 r= the approximation given by Page (1977), (p> 0.5), n1(n1—l) where = x—7.45462/x where — [m1(m1—1)(n1—m1)(n1—m1—1) i I 2 2 x3 = L p (l—p) [y+(y2+3313164)2]/008943 and +2m(n1 —m1) p(l—p) y=O.62657 In [p/(l—p)]. The heritability may then be estimated using Thus what we can estimate is the mean for a the methodology outlined by Bull et a!. (1982) or family but not an individual's value. Using this by the formula of Robertson and Lerner (1949), value for the parental value and computing the parent offspring regression is equivalent to having h2_2'lP) a normally distributed measurement error in the independent variable. The slope of the regression where z is the ordinate on the standardised normal in such cases is less than that computed when no curve which corresponds to a probability p. The measurement error exists (Ricker, 1973; Sokal and standard error of this estimate is given by Rohlf, 1981). Thus the heritability so estimated will be less than that obtained if the individual —p)(l — + (k — SE(h2) =2p(l r)(1 1)r) parental values were known. The advantage of this method over the first described is that maternal effects can be assessed from the regression of mean 11/2 2(N—1) offspring value on single parent. Furthermore, it Lk2c-1)(N-C)] is less sensitive to common environmental effects With characters that show a continuous distri- which can bias analyses based on an analysis of bution the usual method of estimating heritability variance of full sibs. This problem is alleviated to is by mid-parent/offspring regression. With a a degree by the split family design but the above threshold character the problem is that an method is a useful confirmation of the estimate of individual's value is not known. However, if data h2. are available from two generations as in the present study we can use an analogous approach by utiliz- RESULTS ing the family value of the parent in place of its own, unknown value. The rationale for this If there is a genetic component to macroptery we approach is as follows. As outlined above (and in should expect a high correlation between the pro- detail in Roil 1986a) we assume that there is some portion macropterous in the two cages. The intra- continuously varying factor that determines the class correlation coefficients are 0514 for females development of wings. Let the variance within a and 0646 for males. To compute confidence limits family be a- and assume that this is constant we transform r to zandcompute the variance of between families. Consider an individual from z as 1/(n —1.5) where n is the total number of family i with some value T. If T, exceeds the pairs, 178 (Snedecor and Cochran, 1967). The z threshold value T* the animal will be values,corrected for bias, are 0571 and 0712 both micropterous. The probability that an individual with standard error of 00753. In neither case do does not excçcd T* and hence is macropterous is the 95 per cent confidence limits encompass zero given by JQ[(x—p)/o-] dx where Q[(x— and hence we may conclude that there is a sig- jij/o] is 1/o/Ue_1/2[ _.j)/o]2 and p., is the nificant correlation between cages containing mean value of family i. The unit of measurement members from the same family. The data from is arbitrary and hence without loss of generality pairs of different cages have, therefore, been com- we may assume a- =1and T* =0: hence the proba- bined. WING DIMORPHISM IN A SAND CRICKET 225
It is known from a previous study (Roff, 1984) ing parents of different wing morphs can be used that the percentage macroptery varies between the to test for maternal influence on offspring wing sexes. But do families that show a high proportion morph in the following way. If there are maternal of macroptery in one sex do so for the other sex influences there should be a higher proportion of also? The combined results for the F1 and F2 gener- macropterous offspring from crosses of Lx S in ations indicate a very high correlation between the which the female parent is macropterous. There proportion macropterous in the two sexes (r= are no significant differences (for female offspring 0848,t= 166l df= 108, P U) w -J S C) .s S zw .1 •S U) C) 20 0 20 60 80 100 ARCSINEJ% MAC FEMALES Figure2 Percentage macropterous males against the percentage macropterous females from the same family of Gryllusfirmus. The solid line is the 1: 1 ratio and the dashed line the fitted relationship. 226 D. A. ROFF 100 4? • 80 • A •1k AA • 60 AA ••• AI • • 40- Af • A •• L 0>- IA ••. z •• Ui 20 - • •• C A • w A • LL 0- Ui > 100 I- -J 80- ••• 0 60 A A 40- ti.I' A71 A •• 20 A • / A •• A A • 0- I I I 0 20 40 60 80 100 %MACROPTEROUS PROGENY Figure 3Cumulative frequency plots of per Cent macropterous males and females from the three types of cross, S x S (A), S x L (S) and Lx L (A). Each symbol denotes the percentage macropterous progeny from a single family. and females respectively. The two sets of estimates using the mean of the parent's family as its value. are in close agreement. Furthermore, the differen- A probit transformation of the data is required ces between males and females is slight and we which thus excludes two families in which the may reasonably conclude that they estimate a com- proportion macropterous is either 0 or 1. Because mon value. This is, of course, expected from the the midparent value is measured with error the very high correlation between the percentage estimate of heritability will be an underestimate. macropterous females and percentage macrop- The heritability estimates using only the data from terous males (fig. 2). the F1 and F2 generations are 074 and 04O for The second method of estimating heritability males and females respectively (table 2). The is an offspring on midparent regression method associated standard errors are much larger than WING DIMORPHISM IN A SAND CRICKET 227 Table 1Estimates of the intraclass correlation coefficients for (fig. 4). This estimate of heritability is not sig- wing dimorphism in G. firmus by three different methods. nificantly different from those previously derived See text for explanation of the methods (0.62 and 0.68) but is less, as predicted. Method Male Female The covariance analysis can be extended to examine the combined effect of the estimated mid- ANOVA 01917 01763 parent value and the actual wing morph of the x2 01976 01865 MLE 01993 01843 parent on the wing morph of the offspring. The mean offspring value for each sex was regressed on the estimated midparent value using the wing with the previous estimates, due in part to the morphs of the parents as covariants (3 covariates, inprecision with which the parental values are esti- LxL, LxS, SxS). In neither sex is there sig- mated and in part to the reduced sample size. The nificant heterogeneity in the slopes (for female advantage of this method is that the contributions offspring F(2,78) =027,for males F(2,80) 0.06)= of male and female parent can be assessed separ- but there is a significant effect due to the type of ately. The slopes of the regressions are in all four cross (for females F(1,80)= 1344, P<0001 and cases about one half of the estimates using the for males F(l,82)= 1059, P 97.5 S S . "S 90 S Lu . D . -J S > S S 70 S. z . S a. S (I) 50 . U- U- . 0 . z S 30 . S . Ui 10 I I 5 10 20 30 50 70 80 90 95 ESTIMATED MIDPARENT VALUE (%) Figure4 The percentage macropterous males (A) and females (•) against the mean percentage macropterous females in the families of their parents. Data transformed as described in text. Fitted regression lines are shown. heritability under the two photoperiods is approxi- mately the same. Sample sizes, however, are small and hence tests for differences insensitive. A more extensive analysis, with larger sample sizes and more environmental combinations is presently underway. The effect of changes in temperature are more dramatic: the frequency of macropterous males was reduced from 212 per cent (n= 137)at 30°C to 0 per cent (n=57)at25°C. Similarly the 'C frequency of macropterous females declined from 0 80 'C 57'l per cent (n =126)at 30°C to 157 per cent (n =70) at 25°C. Because these data are based on offspring of unknown parentage no estimate of z heritability is possible. However, the data suggest 0C) that h2 is reduced at 25°C compared to 30°C. 'C DISCUSSION Whereaswing length in insects with continuous variation, such as D. melanogaster, is part of a I... • suite of morphological traits, wing dimorphism is more directly connected with patterns of life cycle 20 40 60 adaptation. In a habitat that is very ephemeral, ARCSJNEJ% MAC AT 17L:7D such as sites of rotting fruit or fungi, dispersal is Figure5 The relationship between the per cent macroptery in essential for persistence and selection will favour a family raised in two different photoperiods. Solid line is a population of individuals which are fully capable line of equality, dashed line the fitted regression line. of flight. However, many sites persist for several WING DIMORPHISM IN A SAND CRICKET 229 generations and in such circumstances we might nutritional effects on wing morph (for a review of predict the evolution of non dispersing individuals. population dynamics and field densities see Dixon, This has been demonstrated theoretically (Van 1977). It is also probably reasonable to expect Valen, 1971; Roil, 1975; Järvinen and Vepsäläinen, crowding to affect wing determination in natural 1976) and the decline in the proportion of macrop- populations of leafhoppers but within the Orthop- terous individuals following colonisation of a tera the importance of crowding under natural newly seeded meadow actually observed over time conditions is far from clear except in some species in the coleopteran species, Apion virens, Sitona such as Schistocerca gregaria (Uvarov 1966, 1977). hispidula, S. su1cfrons and Phytonomus nigrirostris The general response to increased crowding is an (Stein, 1977). The genetic basis of wing morph has increase in the proportion of macropterous been established in Sitona hispidula (Jackson, individuals. There are obvious selective advantages 1928) and Apion virens (Stein, 1973; Roff, 1986a). to such a response provided that the increased In both species the trait is determined by a single density is reflected in increases in the succeeding locus with 2 alleles, brachyptery being dominant. generation. For multivoltine species such a correla- The invasion of new habitats by macropterous tion might be expected but for univoltine species individuals of wing polymorphic species of present densities may be poor predictors of carabids has also been observed (Boer, 1970; densities in the following year and hence the Meijer, 1974). Microgeographic variation in the response may have little or no selective advantage. proportion of macropterous individuals that can A second class of genotype-environment inter- be correlated with habitat stability has been recor- actions are those in which the environmental com- ded in leafhoppers (Denno, 1976, 1978, 1979; ponent is some climatic variable such as tem- Denno and Grissell, 1979; Denno et al., 1980; Rey perature or photoperiod. In G. firmus the percent- and Strong, 1983) and such variation has been age of macropterous individuals decreases with observed between species in Gerris spp. (Vep- decreasing photoperiod (fig. 5). Similarly the per- säläinen, 1973, 1974a, b, 1978; summarised in centage macroptery declines with temperature. The Table 11 of Dingle, 1980; Calabrese, 1979). A heritability at the two photoperiods appears to be genetic basis for wing morph determination has approximately the same but the dramatic decrease been demonstrated in both leafhoppers and Ger- in percentage macroptery at the lower temperature ridae (data summarised in Roff, 1986a). In these suggests that heritability may be drastically groups inheritance is polygenic with significant reduced at this temperature. In northern Florida, genotype-environment interaction. from whence this stock was derived, photoperiod At any given site there will be a gradual dim- varies during the year from 1OL: 14D to 14L: 1OD inution over time of the proportion of macrop- and mean daily temperature from approximately terous individuals, due to migration of at least 11°C to 28°C. The air temperature may be mis- some of this morph (Roil 1986b). Such a decrease leading because in a closely related species Gryllus might be suboptimal in species colonising early pennsylvanicus the growth rate at the air tem- successional stages in that the quality of a habitat perature monitored in the field was far less than might be expected to decline over time. As plant observed in free ranging crickets (Roil, unpub- succession proceeds an increase in dispersal rate lished data). It seems likely that the dark colour will be favoured. However, different habitats will of the crickets raises their body temperature above be at different stages in succession and rates of the ambient when exposed to incident radiation succession may vary between sites: thus there may (cf. Begon, 1983). The proportion of macropterous be no single optimal dispersal rate and hence selec- individuals in Northern Florida varies over the tion will tend to preserve genetic variation. A year from 0 per cent to approximately 23 per cent second response to selection for an increased dis- (Veazey et al., 1976; both sexes combined), the persal rate over time is selection for genotype- percentage of macropterous males being con- environment interactions. There are considerable sistently less than that of the females, as found in laboratory data indicating that crowding and/or the present laboratory study. The annual percent- nutrition affects the proportion of macroptery in age of macropterous females in 973 per cent and a variety of species (Honek 1976a). The potential of males 4 15 per cent (data from table 2, Veazey selective advantage of such responses is obvious: et a!., 1976). This low incidence of macroptery however, only infrequently are the laboratory suggests that overall, heritability in the field might results extended to field tests. In the aphids the be quite low. However, the relatively high peak of sedentary mode of life makes it relatively easy to 23 per cent may result in an increase in heritability establish the potential importance of crowding and in those individuals maturing at this time. In 230 D. A. ROFF Gryllus rubens, coexistent with G. firmus, the tion macropterous differs between the sexes argues incidence of macroptery can exceed 50 per cent against this interpretation although such a (Veazey et a!., 1976). In the subspecies of G.firmus, difference might be due to hormonal differences G.f bermudensis field collections indicate a per- associated with sex. More research on the possible centage macroptery of "at least 30 per cent" costs of being winged in males is clearly needed. (Kevan, 1980). Thus a high heritability may poten- tially be realised under natural conditions. Acknowledgements I should like to thank Ms Catherine Helik Environment-genotype interactions may be a for her invaluable aid in the rearing of the crickets and Drs consequence of the physiological basis of wing Kurt Sittman and J. A. Endler for comments on the manuscript. morph determination (Roff, 1986b). The sig- This study was supported by a N.S.E.R.C. operating grant nificance of this variation is that, providing it has A7764. a genetic component, selection can produce an appropriate rate of dispersal. Responses to habitat deterioration have an obvious selective advantage: REFERENCES responses to photoperiod and temperature may be selected and maintained because they generate the ALEXANDER,R. D. 1968. Life cycle origins, specialization and related phenomena in crickets. Quart. Rev. Biol. 43, 1-41. appropriate rate of density-independent dispersal. ANDREWARTHA, H. G. AND BIRCH, L. C. 1954. The distribution The proportion of macropterous males in G. and abundance of animals. Univ. 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