The genetic basis of the trade-off between calling and wing morph in males of the cricket Gryllus firmus.
The advantage to being flight capable is the ability to move over large areas and in three dimensional space (Roff 1990a). However, although producing and maintaining the long wings that macropters possess is probably not energetically significant, the production and maintenance of the massive flight muscles is energetically expensive (Roff 1989; Mole and Zera 1993; Tanaka 1993). Although in some cases of dimorphic variation one morph may have a reduced fitness and be adopting the "best of a bad lot" strategy (Eberhardt 1982; but see Roff 1996), the wide occurrence of dimorphisms suggests that, in general, the dimorphism is maintained in the population as a consequence of trade-offs (Gross 1984; Roff 1984; Hazel et al. 1990; Roff and Fairbairn 1993; Roff 1996). Wing dimorphisms appear to be maintained by a trade-off between resources devoted to dispersal (wings, flight muscles, and flight fuels) and those devoted to reproduction (Roff 1984; Denno et al. 1991; Roff and Fairbairn 1991; Zera and Denno 1997). In many species of macropteorus insects, the flight apparatus is not maintained throughout adult life (wings may be removed and flight muscles histolyzed), and therefore the trade-off may be important only during the time over which the flight apparatus is functional.
Most of the studies of the costs of macroptery in wing-dimorphic insects have been done using females. In general, micropterous females reproduce earlier and have a higher fecundity than macropterous females (Roff 1986a; Denno et al. 1989; Roff and Fairbairn 1991). These differences are very large in the sand cricket, Gryllus firmus: micropterous females reproduce significantly earlier after the final moult (two days) and produce 60% more eggs in a six-week period than do macropterous females (Roff 1984). Physiological studies have shown that fecundity differences in G. firmus females are due to the allocation of resources to reproduction in the SW (micropterous) morph and those to flight apparatus maintenance in the LW (macropterous) morph (Mole and Zeta 1994a,b).
For a trade-off to affect the evolution of wing dimorphism, there must be a genetic correlation between the traits involved, that is, between wing morph and reproduction. Without a genetic correlation, selection for an increase in proportion macroptery will not be accompanied by a decrease in fitness-related traits and will, therefore, result in a monomorphic winged population. Genetic correlations between wing morph and fecundity have been demonstrated in female G. firmus (Roff 1990b, 1994c) and the cricket Allonemobius socius (Roff and Bradford 1996; Roff et al. 1997), indicating that the trade-off will modulate the evolution of these two traits.
Although the existence of costs to macroptery are well [TABULAR DATA FOR TABLE 1 OMITTED] documented in female insects, only a few examples of costs have been studied in male insects. Phenotypic trade-offs to macroptery have been shown to exist in thrips, coleopterans, planthoppers, waterstriders, and a hemipteran (Crnokrak and Roff 1995; Fairbairn and Preziosi 1997). The above-mentioned studies have demonstrated phenotypic trade-offs between morphological and life-history traits in male insects, but to date no study has examined the genetic basis of these trade-offs.
In G. firmus, as with many other Orthopterans, males are relatively sedentary as adults (Alexander 1968; Dadour 1990; Cade and Cade 1992) and attract females by calling. A number of components of calling are known to be important cues for female attraction, of which one of the most important appears to be total time spent calling (Table 1). Studies on Orthopterans have shown that the likelihood of attracting a female is typically proportional to call duration (for references, see Table 1). Calling is energetically demanding, requiring on average, a 10-fold increase in metabolic rate (data for seven species from Table 1 of Bailey et al.  and one species from Forrest 1991b). A phenotypic trade-off has been demonstrated in male G. firmus, with micropterous males calling longer and attracting more females than macropterous males (Crnokrak and Roff 1995, in press). Wing form in G. firmus has a significant and high heritability ([h.sup.2] = 0.65; Roff 1986b). In G. integer, call bout length has a significant and high heritability (0.75; Hedrick 1988, 1994), whereas Cade (1981) found in the same species that mean nightly time spent calling also has a significant heritability (0.50). These data suggest that there will be additive genetic variance for call duration in G. firmus, and that a genetic correlation between wing morph and call duration is feasable (i.e., both [h.sup.2] are high). Without a genetic correlation between them, the evolution of wing dimorphism and call duration will not be jointly constrained. A significant negative genetic correlation between calling and wing morph would mean that selection acting on one trait would result in a correlated response of the other, a necessary requirement for any tradeoff to be evolutionarily important (Stearns 1989; Roff 1994c).
In the present study we examined the genetic basis of the trade-off between wing morph and calling behavior in G. firmus, addressing two main questions: (1) are the traits involved in the trade-off (call duration, wing morph and flight muscle condition - a measure of the degree of histolysis) significantly heritable? and (2) is there a significant genetic correlation between call duration and wing morph and call duration and flight muscle condition?
MATERIALS AND METHODS
Species Description and Methods of Rearing
Gryllus firmus is a large (live weight, = 0.75 g), ground-dwelling cricket found in the American Southeast as far north as Connecticut (Alexander 1968; Harrison 1985). It is usually found in early successional and sandy areas, which being impermanent favor the evolution of wing dimorphism (Roff 1990a, 1994b). Individuals in this experiment originated from approximately 40 individuals (20 males, 20 females) from a locality in northern Florida (Roff 1986b). Stock crickets were maintained in the laboratory at approximately 100-300 breeding adults at a temperature of 25-30 [degrees] C for approximately 38 generations before being used for the behavioral experiments. Crickets used for the experiments were maintained as nymphs in disposable mouse cages (29 x 19 x 13 cm) in incubators set at a photoperiod of 15 h light, 9 h dark and at a temperature of 28 [degrees] C with ad libitum food and water. After one week in the mouse cages, nymphs were placed in 4-L buckets (diameter = 21 cm; height = 15 cm) at a density of 60 nymphs per bucket. Food consisted of crushed Purina rabbit chow provided ad libitum. Water was provided by a soaked cheesecloth wick connected to a water reservoir in a second bucket into which the first bucket was suspended. On the day of their final ecdysis (the day nymphs became adults), individuals where removed from these rearing buckets and placed in individual quarters containing food and water until they were six days old, at which time they were used in the experiment.
General Setup. - Figure 1 shows the T-maze used for the behavioral experiment. Each male was housed in an individual glass jar and monitored for call duration and whether they attracted a female. Each glass jar was placed in a bucket that was connected to two other buckets by plastic 2.5-cm diameter tubing, which thereby formed a T-maze. Eight T-mazes were used, all of which were placed in incubators set at a 15:19 L:D photoperiod and 28 [degrees] C. For each T-maze, two males (one micropterous [SW], one macropterous [LW]) and a single female (either LW or SW, chosen at random) were placed in separate buckets as indicated in Figure 1. The 2.5-cm tubing that interconnected all three buckets allowed the females free access to the males' quarters. Cones placed on the end of each tube leading to a male's quarters prevented the female from exiting the bucket of the male she first entered. The jars housing the males were painted black to prevent the male and female from seeing each other. Wire mesh covered the top of each jar allowing females to hear the calling males. A continuous playback of cricket calling was used to provide a constant background (Cade and Wyatt 1984).
Male calling was monitored by Realistic tie-clip 33-105 microphone (frequency response, 50-15,000 Hz) placed in each male's jar. Microphones were connected to an analog-to-digital converter relay system monitored by a computer that recorded the time of each incoming signal. The computer scanned the relay system once every second. Chirp length averages 154 msec (Webb and Roff 1992) and are repeated in bout lengths generally exceeding one second (average bout length = 1.47s; PC, pers. obs.). Each microphone gain was set at a level that would trigger the relay system only when the occupant of the jar called and would not be triggered by the background call or the call of neighboring crickets. A simple binary code was used by the computer to record when a male called (1 = calling, 0 = not calling). Every male was monitored for 23.5 h, on day 6 as adults. Day 6 was picked as the best one-day compromise because calling increases up to day 6 and then changes little afterward (Crnokrak and Roff, in press). Recording began at 1300 h each day and ended at 1230 h the next day (30 min was spent on maintaining the food and water levels and cleaning the T-maze). After daily maintenance was completed, the computer was reset and monitoring recommenced.
Breeding Design. - Sires were obtained from eggs laid in earth dishes from the general breeding stock of crickets (see above for description). The earth dishes were placed in disposable mouse cages in incubators set at 15:9 L:D and 28 [degrees] C. Nymphs were reared in 4-L buckets (60 in each) and maintained under the same photoperiod and temperature conditions as the eggs. Once adult, the males were placed in individual quarters until six days old, at which time they were monitored for call duration and female attraction. Eleven SW and 11 LW sires were monitored (sires were paired with males that were not used for the genetic experiment; sample size for sires = 22). After measurement of call durations, the sires were placed in individual buckets and allowed to mate with a female (morph picked at random) for approximately one week. Females oviposited their eggs in soil in Styrofoam cups during this time, which were incubated under the same environmental conditions as before. These nymphs ([F.sub.1] generation) were maintained in 4-L buckets until adults, at which time they were raised individually until six days old and monitored for time spent calling and female attraction. From each family, five SW and five LW male offspring were monitored (thus the total sample size for the female choice experiment was 22 sire pairs + 10 x 11 offspring = 132). The remaining crickets from each family were raised until adulthood to obtain an estimate of proportion macroptery for each family. All male crickets used in the experiment were preserved by freezing for muscle analysis.
Muscle Condition Analysis. - Preserved sires and offspring were thawed and dissected to determine weight and condition of their dorsal longitudinal flight muscle. The dorsal longitudinal flight muscles (DLMs) are situated immediately ventral to the dorsal portion of the mesothorax (Pfau and Koch 1994). Muscle condition was determined visually by comparing muscle color on a three-point scale: beige white (0), pale pink (1), and brick red (2). Muscle color is an indicator of functional (red) or nonfunctional (white) flight muscles (Ready and Josephson 1982). All color tests were performed by one person (PC) to eliminate any variation in vision perception among experimenters. Muscles were then dissected out of the crickets and dried for one week at 60 [degrees] C and weighed to an accuracy of 0.0001 g. Although all male crickets were dissected, only LW individuals had measurable flight muscles.
Descriptive Statistics. - We used a t-test to determine if significant differences exist between morphs in call duration (both sires and offspring) for the 23.5 h of monitoring. Because the a priori prediction is that SW males will call longer than LW males, the t-test was one-tailed.
We assessed female choice using a goodness-of-fit test; because the prediction is that SW males will attract more females than LW males, the test was one-tailed (critical [[Chi].sup.2] = 2.71).
To examine the relationship between call duration and the probability of attracting a female we used the model:
P = b [C.sub.SW]/[C.sub.SW] + [C.sub.LW] = bC, (1)
where P is the probability of a female choosing the SW male, [C.sub.SW] is the call duration of the SW male, [C.sub.LW] is the call duration of the LW male, and b is a constant. If the probability of attracting a female is proportional to the relative call duration (C), then b = 1. If, as suggested by previous analyses (Crnokrak and Roff 1995) females show a bias for SW males then b [greater than] 1. Because the maximum value of P is one, if the bias is sufficiently great the relationship may be curvilinear with an asymptote at one. No such curvature was found in the present analysis and hence we shall restrict our attention to the above model. Because single females were used in each trial, P is a binary variable taking values of zero (female chose the LW male) and one (female chose the SW male). Such data do not fulfill the assumptions of least-squares regression and, therefore, we used a maximum-likelihood approach. The likelihood, L, for a sample in which the number of SW and LW males chosen is [n.sub.1] and [n.sub.0], respectively, is:
[Mathematical Expression Omitted]. (2)
The slope, b, was estimated as that which maximized the above likelihood. To provide a test of the slope we used the 95% confidence interval estimated using Wald's method (Wilkinson 1996, p. 452). In addition, the above model was fitted using least squares by minimizing the mean square error.
We used ANOVA to determine if differences exists between DLM weight among muscle color groups. Because the a priori prediction is that functional muscles (group 2) will be larger than nonfunctional muscles (group 0), the test was one-tailed.
Heritability Estimates. - Full-sib heritability estimates were calculated using nested (cages nested within families) ANOVA and the jackknife (Simons and Roff 1996). As both estimates gave almost identical results we present only those from the ANOVA. Heritability estimates calculated were: time spent calling (SW and LW separate, and SW + LW), wing morph (using the threshold model, for details, see Roff 1997), and DLM weight of macropterous males. Full-sib estimates of heritability include (Becker 1995):
[Mathematical Expression Omitted], (3)
where [V.sub.a] = additive genetic variance, [V.sub.d] = dominance variance, and Vi = epistatic variance. Cage effects were nonsignificant and, therefore, cages were combined.
In addition to the full-sib estimates, we calculated offspring-parent heritability estimates for call duration. Because these estimates include only [V.sub.a] in the numerator, a comparison of full-sib and parent-offspring heritability estimates allows us to determine the contribution of nonadditive effects to the total genetic variance. The offspring-parent heritability estimate for call duration was calculated using a regression of mean offspring values on mean sire values; where the dependent variable, offspring call duration = (SW mean call per family) x (proportion SW in family) + (LW mean call per family) x (proportion LW in family); and the independent variable = sire call duration. In addition to the above analysis we also ran the regression separately for SW and LW males (mean SW offspring call duration regressed on SW sire call duration, etc).
Phenotypic Correlation Estimates. - We calculated phenotypic correlations for call duration and wing morph and; LW call duration and DLM weight. Correlations were calculated using offspring values for both estimates. Because family sizes were equal, phenotypic correlations were calculated using a general linear regression of call duration on wing morph and DLM weight.
Genetic Correlation Estimates. - We calculated genetic correlations for LW call duration and wing morph; SW call duration and wing morph; LW call duration and DLM weight; and call duration between morphs. Because a fixed number of LW and SW offspring per family (irrespective of proportion macroptery in the family) were measured, genetic correlations could not be estimated in the usual manner (Roff and Bradford 1996). However, genetic correlations from full-sib data can be estimated, at least approximately, by the Pearson product moment correlation between family means (Via 1984; Roff and Preziosi 1994). Mean values per family were calculated by first calculating mean values per cage (as described above) and then averaging across cages.
Standard errors values for the correlation estimates were calculated using (Becker 1995):
SE = [-square root of 1 - [r.sup.2]/n - 2]. (4)
Call Duration. - SW males had significantly longer call durations than LW males (t = -11.404, df = 216, P [less than] 0.0001); SW males called for 0.86 [+ or -] 0.01 h and LW males for 0.64 [+ or -] 0.01 h.
Female Attraction. - SW males attracted 83 of 131 (63%: one female did not move reducing the total sample size by one) females that made a choice for a male in the T-mazes, whereas LW males attracted 48 of the 131 (37%) females (total females that moved = 110 [offspring tests] + 21 [sire tests-1 female that did not move]). As predicted, SW males attracted significantly more females than LW males ([[Chi].sup.2] = 4.68, P [less than] 0.01).
Call Duration and Female Attraction. - There was a significant effect of relative call duration on the probability of attracting a female (95% confidence interval excluded 0; least-squares estimation gave r = 0.83, P [less than] 0.1 x [10.sup.-6]): because the SW male called longer than the LW male, the females chose the SW male more frequently. The slope for the model was significantly greater than one ([Mathematical Expression Omitted] confidence interval: 1.05-1.28; by least-squares confidence interval: 1.01-1.27), indicating an effect of male morph type in addition to relative call duration on the probability of attracting a female. Although there is a difference between the predicted slope value of one and the calculated value of 1.17, it is not substantial, indicating that relative call duration is much more important to female choice than male morph type (i.e., substituting a C-value of 0.57 (mean relative call duration for all crickets) into the model gives P = 0.67, indicating that the relative effect of male morph type is 0.10 compared to the relative call duration effect of 0.57).
TABLE 2. Summary of heritability estimates using the full-sib and parent-offspring analysis. Trait [h.sup.2] [+ or -] SE n P Full-sib estimates SW call duration 0.68 [+ or -] 0.21 110 0.002 LW call duration 0.81 [+ or -] 0.21 109(a) 0.002 SW + LW call 0.75 [+ or -] 0.33 219 0.04 Wing morph 0.22 [+ or -] 0.07 44(b) 0.01 DLM weight 0.38 [+ or -] 0.09 109 0.007 Offspring-parent estimates SW call duration 0.61 [+ or -] 0.39 11 0.151 LW call duration 1.07 [+ or -] 0.34 11 0.012 SW + LW call 0.72 [+ or -] 0.13 22 0.0001 a,b Note: sample sizes change definition depending on trait type; all of the full-sib estimates are individual values except for wing morph, which is mean proportion macroptery per cage (two cages per family); offspring-parent estimates for SW and LW call duration are regressions of mean offspring values on sire values (SW offspring on SW sires and LW offspring on LW sires): SW + LW call duration is a regression of mean offspring values on sire values for both morphs. Where a = 110 - 1 (one LW male died during experiment), b = 22 families x 2 cages per family = 44.
DLM Weight. - The mean [+ or -] SE DLM weight for the three muscle conditions were: 0.0029 [+ or -] 0.0006 g (beige white, n = 21); 0.0058 [+ or -] 0.0009g (pale pink, n = 22); 0.0075 [+ or -] 0.0003g (brick red, n = 67). Muscles with different colors had significantly different mean weights (n = 110, [F.sub.df-1] = 43.283, P = 0.0001). As predicted, functional red muscles were heavier than nonfunctional white muscles.
Phenotypic Correlations. - Both phenotypic correlations were highly significant; call duration and wing morph, r = -0.61 [+ or -] 0.05, n = 218, df = 1, P = 0.0001; LW call and DLM weight, r = -0.32 [+ or -] 0.09, n = 109, df = 1, P = 0.001.
TABLE 3. Summary of genetic correlation estimates ([r.sub.A] [+ or -] SE). All correlations are significantly different from zero. Wing morph DLM weight LW call duration -0.46 [+ or -] 0.20 -0.80 [+ or -] 0.14 SW call duration -0.68 [+ or -] 0.16
Heritability and Genetic Correlation Estimates
All heritability estimates were significant, except for the offspring-parent heritability of call duration for SW crickets (Table 2). The full-sib and offspring-parent heritability estimates for SW and LW call duration, SW + LW call duration, and DLM weight were very similar, indicating that nonadditive genetic variance (dominance and epistasis) contributes relatively little to the heritability estimates.
Three of the four genetic correlations were highly significant (Table 3). As predicted, with an increase in proportion macroptery in a family the mean SW and LW call duration decreases [ILLUSTRATION FOR FIGURE 2 OMITTED]. In addition, for LW males in each family, as the mean DLM weight increases the mean LW call duration decreased [ILLUSTRATION FOR FIGURE 3 OMITTED]. The significant genetic correlation demonstrates a genetic basis to the trade-off. The genetic correlation between wing morphs for call duration was nonsignificant ([r.sub.A] = 0.13 [+ or -] 0.22, n = 22, df = 1, P = 0.561), suggesting that selection for call duration in one morph will not be constrained by the other morph. However, the large standard error does not preclude an evolutionarily important genetic correlation: a larger sample size is required to answer this question.
Although flight capability can be advantageous under conditions of habitat change, it is not without costs. Producing and maintaining the flight apparatus (wings, wing muscles, and flight fuels) is energetically expensive (Mole and Zera 1993, 1994a,b; Tanaka 1993; Zera et al. 1994). The energy needed to maintain the flight muscles is hypothesized to constrain resources that could be used for calling in males. Previous studies on male G. firmus have shown the existence of a phenotypic trade-off between macroptery and calling (Crnokrak and Roff 1995) and that the trade-off exists under both ad libitum food and resource restriction (Crnokrak and Roff, in press). As in the previous study, in the present study we found a significant phenotypic trade-off between macroptery and the probability of attracting a female: SW males attracted a significantly greater number of females than LW males. This difference is due to differences in relative call duration between the morphs: SW males called longer during a 24-h period than LW males. In addition, females preferred the SW male even when call effects were accounted for in the model. On a genetic level, we found that the traits involved in the trade-off (call duration, wing morph, flight muscle weight) are all significantly heritable. The genetic correlations between the traits (LW call duration and wing morph, SW call duration and wing morph, LW call duration and flight muscle weight) were also all significant and all negative. This is, to the best of our knowledge, the first study of trade-offs between a dimorphic trait and fitness-related traits in males to have demonstrated the existence of a genetically based trade-off.
Trade-offs are a central facet of life-history evolution (Stearns 1977, 1989; Bell 1980; Reznick 1985; van Noordwijk and de Jong 1986; Pease and Bull 1988). The study of trade-offs is important because traits rarely evolve as single units. In addition, because there is usually a finite amount of resources available to be allocated to different functions in an organism, competition among traits for resources is inevitable (Pease and Bull 1988). The most commonly measured trade-offs are phenotypic because analyses on this level are relatively simple compared to a genetic analysis (Stearns 1989). A genetic analysis of trade-offs requires heritability estimates of the individual traits involved and genetic correlation estimates between these traits. The present study has fulfilled both of these requirements. Our comparison of full-sib and parent-offspring heritability estimates revealed that nonadditive effects contribute little to the heritability estimates; in addition to the relatively high heritability estimates, this would mean that the traits in question will rapidly respond to selection.
The genetic correlations between call duration and wing morph reported here indicate that the trade-off is relatively high in magnitude and negative. Therefore, in a relatively unstable habitat, although selection will favor macropterous males, because of the negative genetic correlation between wing morph and call duration, selection favoring the increase in proportion macroptery in a population will result in a mean decrease in call duration among the macropterous males. Thus, macropterous males from a population that is predominately micropterous will have relatively longer call durations than macropteorus males from a population that is predominately macropterous. Because longer-calling males have a higher probability of attracting females, variation in proportion macroptery will result in changes in the relative fitnesses between micropterous and macropterous males. In this way, these genetically based trade-offs will mediate the evolution of wing dimorphism in a population.
To fully understand a biological system, it is crucial to examine the phenomenon in question on all possible levels. The behavioral trade-off between macroptery and calling behavior in G. firmus males has been studied by us on a phenotypic and genetic level. Previous studies have shown that a behavioral trade-off exists and that this trade-off is affected by available resources (Crnokrak and Roff 1995, in press). Although the present study examines the trade-off on the single most important level, the genetic level, there is still a lack of information concerning how genetics is translated into the phenotype. Because the trade-off is believed to be a resource-based trade-off where a finite amount of resources must be partitioned between maintaining the flight apparatus and calling, it is important to verify this hypothesis by examining the trade-off on a physiological level. A physiological trade-off can be negated on a phenotypic level if an organism has the ability to mediate its behavior to compensate for a shortfall in metabolic resources. In G. firmus, macropterous females partially compensate on a behavioral level for the physiological trade-off between macroptery and egg production by eating more food than micropterous females (Mole and Zera 1994a). Although in one experiment with G. firmus LW females appeared to compensate for the physiological trade-off by eating more than SW females (Mole and Zera 1994a), this has not been observed in four other experiments with G. firmus (Roff 1984, 1989, 1994a; Roff et al. 1997) and one with G. rubens (Mole and Zera 1993). We are presently analyzing data from the physiological experiments to determine which traits are involved in the macroptery-call trade-off in male G. firmus. To date, we have determined that significant negative genetic correlations exist between call duration and flight muscle weight (this paper) and flight muscle weight and proportion macroptery (Crnokrak and Roff, unpubl. data). As hypothesised, these results confirm that the phenotypic trade-off is underpinned by a trade-off on a physiological level.
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|Author:||Crnokrak, Peter; Roff, Derek A.|
|Date:||Aug 1, 1998|
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