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Geographical variability in ecophysiological traits controlling dormancy in Chrysopa oculata (Neuroptera: Chrysopidae)
J. fnsect Physiof. Vol. 33, No. 9, pp. 627-633, 1987 Printed in Great Britain. All rights reserved
Copyright 0
C022-1910/87 $3.00 +O.OO 1987 Pergamon Journals Ltd
GEOGRAPHICAL VARIABILITY IN ECOPHYSIOLOGICAL TRAITS CONTROLLING DORMANCY IN CHRYSOPA OCULATA (NEUROPTERA: CHRYSOPIDAE) JAMESR. NECHOLS’, MAURICEJ. TAUBER~ and CATHERINE A. TAUBER~ *Department of Entomology, Kansas State University, Manhattan, KS 66506 and TDepartment of Entomology, Comstock Hall, Cornell University, Ithaca, NY 14853-0999, U.S.A. (Received 22 July 86; revised 6 January 1987)
Abstract-Dormancy in Chrysopa oculata, a multivoltine species, is controlled by reponses to photopcriod and temperature. Variation in both the critical photoperiod for diapause induction and the duration of diapause is positively related to the latitudinal origin of the population. The incidence of photoperiodically induced diapause also varies geographically; at 24°C the southern-most population is more variable for diapause induction than the northern populations. By contrast, there is little interpopulation variation in thermally determined rates of post-diapause development. The results suggest that the lower threshold for development and the thermal requirements above the threshold may be functionally correlated. Key Word Index: Diapause, photoperiod,
geographical variation, thermal responses, Chrysopa
INTRODt_JCTION While undergoing dormancy, insects progress through a series of distinct physiological phasesdiapause induction, maintenance and termination, post-diapause quiescence, and post-diapause development. Each of these phases is characterized by a set of ecophysiological responses which appear to evolve in a coordinated manner to adapt insects to the seasonally variable physical and biotic conditions of their local environment (see Tauber et al., 1986). Therefore, knowledge of the genetic variation and adaptive significance of the response patterns expands the understanding of the physiology of dormancy. In theory, all of the response patterns that control dormancy should be subject to equivalent evolutionary modification over space and time. But, in reality, some appear to exhibit much greater variation than others. For example, among geographically widespread insect species, the photoperiodic induction of diapause is generally highly variable, whereas the species-specific diapausing stage and the thermal regulation of developmental and reproductive rates are relatively conservative in their variation (Danilevskii, 1965; Taylor, 1981; Tauber et al., 1986). This biased pattern of intraspecific variability raises the question of how ecophysiological responses interact with each other. Do the various responses vary independently or are they genetically or functionally correlated? Are some traits innately more variable than others? Do genetic correlations (e.g. linkage) between physiological traits set limits to the expression of variation among the traits? Resolution of these questions is necessary for understanding how the physiological adaptations underlying dormancy
evolve-the rates of their evolution, the limits to their evolution, etc. Numerous studies with insects have examined variability in a single seasonal response pattern-the critical photoperiod for diapause induction being the most common (see Tauber et al., 1986). However, very few have examined variation in sets of seasonal responses (e.g. Istock 1978, 1981; Kidokoro and Masaki, 1978; Masaki, 1978a, b, 1979; Dingle et al., 1980a, b; Holzapfel and Bradshaw, 1981; Hegmann and Dingle, 1982; Tauber and Tauber, 1982, 1986). Thus, to initiate a study of the relationship among seasonally important ecophysiological traits, we investigated the pattern of geographical variability in a suite of responses that control dormancy from its onset through its termination in a widespread North American species of insect predators. We examined various aspects of diapause and post-diapause development: specifically the photoperiodic induction of diapause, the innate duration of diapause, the photoperiodic influence on diapause duration, and the thermal regulation of postdiapause development. MATERIALSAND METHODS Experimental animal Chrysopa oculata Say is multivoltine throughout its range, which comprises all of the contiguous United States, southern Canada, and parts of northern Mexico. Adults emerge in the spring; reproduction and development take place throughout the summer and autumn until frosts occur (Tauber et al., 1987). Both adults and larvae are predaceous, so the initiation of oviposition and the timing of the summer generations depend on temperature and the availability of prey (Tauber et al., 1987). 627
JAMESR. NECHOLS et al.
628
Table I. Localitv data for neoaranhical Domdations of Chryso~a oculalo tested in this studv Locality
Latitude
Grand Beach, Lake Winnipeg, Manitoba, Canada Brownstown, 15 mi. SW Yakima, Yakima Co., Washington Ithaca, Tompkins Co., New York Dinosaur National Monument (Green River Campgrd.), Uintah Co., Utah IOmi. W. Loveland, Larimer Co., Colorado Manhattan, Riley Co., Kansas Lubbock, Lubbock Co., Texas College Station, Brazes Co., Texas Quincy, Gadsden Co., Florida 17mi. SE Saltillo. Coahuila, Mexico
50”34’ N 46”31’ N 42”26’ N 40”27’ N 40”24’ N 39”ll’N 33”35’ N 30”38’ N 30”34’ N 25”30’ N
C. ocufata overwinters as mature, diapausing thirdinstar larvae (“prepupae”) within cocoons. Diapause is induced primarily by photoperiod; exposure of second and third-instar larvae to short daylengths/ long nightlengths induces diapause (Propp et al., 1969). Thus, C. oculata is a “long-day species” (Type 1 of Beck 1980). As is typical of most long-day species, low temperatures enhance the diapauseinducing effects of photoperiod (Tauber et al., unpublished). Thus, if summer temperatures are low, diapause is induced earlier than if conditions remain warm. Once induced, diapause persists under short daylengths in the laboratory for about 3-4 months. Subsequently, it terminates spontaneously, i.e. apparently without external stimulus. Exposure to cold is not necessary for diapause termination or the successful completion of post-diapause development in this species (Propp et al., 1969). Postdiapause development comprises two stages: the prepupal stage which extends from diapause termination by the third-instar larvae to the larval-pupal moult, and the pupal stage which lasts from the larval-pupal moult to adult emergence. Experimental procedures
Adults of C. oculata were collected at numerous localities throughout the range of the species (Table 1). The number of fertile females collected was greater than ten for each population except three (Dinosaur National Monument, Utah, Loveland, Colorado, Saltillo, Coahuila), each of which had three mated females. All tests were run with first-generation offspring of field-collected adults. Be-
Elevation (ft) 764 1066 815 -8000 _ 5000 1066 3240 308 187 6800
cause they are cannibalistic, larvae were reared in individual shell vials. The larval diet consisted of pea aphids, Acyrthosiphon pisum (Harris). Adults were provided pea aphids and a proteinaceous diet (a 1: 1: 1: 1 volumetric mixture of Wheast@, protein hydrolysate of yeast, sugar and honey). At 24”C, nondiapause individuals pupate within 10 days of spinning. Thus, we considered individuals that did not pupate within this period to be in diapause. In almost all cases, diapausing larvae did not pupate until they had been in the cocoon for 70 days. To examine the variability in photoperiodic induction of diapause among the ten geographical populations, we reared individuals from each population under a range of constant photoperiods from light-dark 10: 14 to light-dark 16:8 (Temperature = 24 f 1’C) (Table 2). We recorded the incidence of delayed pupation under each condition and used these data to determine the critical photoperiod. For all populations except Saltillo, we followed standard procedures and designated the critical photoperiod as the photoperiod at which 50% of the larvae entered diapause. Because even under the shortest daylengths tested, only a proportion of Saltillo individuals entered diapause, we used the midpoint between the maximal and minimal response as the critical photoperiod for this population. This value represents 50% of the individuals that are susceptible to diapause induction under our laboratory conditions (24 + l”C, surplus of food). To determine the variability in the length of diapause and to examine the relationship between the critical photoperiod and diapause duration, we main-
Table 2. Geographical variation in photoperiodic induction of diapause among North American populations of Chrvsooo oculata (Temo = 24 + 1°C) IO Geographical
population*
Grand Beach, Manitoba Brownstown, Washington Ithaca, New York Dinosaur Nat]. Mon., Utah Loveland, Colorado Manhattan, Kansas Lubbock, Texas College Station, Texas Quincy, Florida Saltillo. Coahuila
Daylength per 24 hours 12 13
II
14
IS
16
% Diapause (No. individuals)
-
100(49) 100(25) lOO(57) lOO(12) 1OO(24) lOO(l2) lOO(12) 50(8)
loo(l6) loo(ll) 33I6)
WW W22) loo(62) loO(16) 86(l4) loo(38) loo(l2) 10009) 92(12) o(8)
lC$) 36(44) lOO(20) 93(15) 13(38) 27(11) 80(20) 36(11) o(8)
65(11) 90(20) o(63) 25(24) lo(l0) o(37) 002) o(l8) o(l2) M8)
*See Table 1 for full locality data. Two other photoperiods were tested for the Ithaca, New York, population: light-.iark (36); light-dark 13.5: 10.5 = 3% (37).
‘X18) WV O(43)
ow
O&l, 005) -
:$z; O(37)
O(39)
00
12.5: 1I .5 = 100%
Geographical variability
629
Table 3. Relationship between diapause-inducing/-maintaining photoperiod and diapause duration (time to pupation, which includes a short period of post-diapause development) in North American populations of Chrysopa oeulara (Temp. = 24 + 1°C) Duration of diapause P + SD days (No.) Geographical
10: 14
population*
Grand Beach, Manitoba Brownstown, Washington Dinosaur, NM., Utah Loveland, Colorado College Station, Texas Quincy, Florida
11:13 -
125 + 23abt (49) 91 f 25a (44) -
-
72 + 2Oab (12) 84 * 27a (10)
83 rt 12a (16) 85 k 9a (9)
Photoperiod light-dark 12: I2 106 k 23at (18) 112+ 16b (20) 77 5 24a (16) 82+ 16b (12) 65 k 17b (20) 66 * 29a (11)
13:ll
131 + 28a (20) 96+4la 08) 103 + 19a (13) 74k llab (16) 61 + 15a (3)
14:lO 103 f 30a (11) 139k28a (17) 94i lla (5) -
*See Table 1 for complete locality data. tValues within rows followed by same letter are not significantly different at P = 0.05 [f-test (LSD)].
tained diapausing individuals under their diapauseinducing daylengths until pupation (Table 3). Every day for 2 weeks after spinning, cocoons were checked for pupation; subsequently, they were examined every third day. The larval-pupal ecdysis was used as an indicator that diapause had ended; thus our estimates of diapause duration (Tables 3 and 4) include an 8 to IO-day period of post-diapause development. To compare thermal requirements for postdiapause development among the geographical populations, we reared individuals from seven localities under short-day conditions (lightdark 10: 14, 24 + 1’C) to induce diapause. Three weeks after the larvae had spun cocoons, we transferred them from 24 to 4 + 1°C (light-dark 10: 14), where they were held untidiapause ended-approximately 4 months. Subsequently, we divided the cocoons among five conditions consisting of a range of temperatures from 15.6 to 24°C (all f 1”) under light-dark 16 : 8 and 24°C under light-dark 10: 14 (Table 4; Appendix 1). Each condition was replicated three times. Developmental times (in days) were recorded for the two post-diapause stages (the prepupal stage-from the day of transfer until larval-pupal ecdysis, and the
pupal stage-from larval-pupal ecdysis to adult emergence). The individuals under short daylengths served to determine if diapause had ended by the time the cocoons were transferred to the temperature conditions. In the six populations tested, photoperiod had no significant effect on the time to pupation after cocoons were transferred from the cold to a development-favouring temperature [24 + l“C] (t-test; P = 0.05). Thus, diapause had ended before we began our tests on post-diapause development. In analyzing the relationship between temperature and development, we computed the reciprocal of the development times (y-axis) at every temperature (x-axis for individuals from each strain and then fitted these data to linear regression curves using the least squares method. We estimated the lower thermal threshold for development, t, by linear extrapolation through the x-axis (temperature), and we derived the thermal constant, K, by the equation K = y(d - t), where y = mean developmental time in days and d = temperature (“C). We used the analysis of covariance procedure (SAS Institute 1982) to test for interpopulation differences in the slope and the
Table 4. Geographical variation in diapause duration (time to pupation, which includes a short period of postdiapause development) and in the thermal requirements (I and K) for postdiapause development among North American populations of Chrysopo oculara (see Appendix for stage-specific data)
Geographical
population*
Grand Beach, Manitoba Brownstown, Washington Ithaca. New York Dinosaur Nat]. Mon., Utah Loveland, Colorado College Station, Texas Quincy, Florida
Duration of diapause X f SD days (No.)t 106 & 23(18)b 125 + 23(49)a 93 f 1l(33)c 91 f 25(44)c 82 + 16(12)cd 72 f 20(12)d 80 f 18(37)cd
Thermal requirements for post-diapause development r(C + SE) K(D-D&SE) 9.9 +_4.6 9.8 k 1.8 12.2 f 2.2 11.322.4 9.2 i 3.8 11.4* 1.4 ll.Ok2.7
351 + 45 276112 228 f 32 253 f 26 332 f 51 253 k 13 261 & 34
*See Table I for complete locality data. tValues followed by same letters are not significantly different at P = 0.05 (Duncans’s Multiple Range Test). All populations were maintained under light-dark 10: 14; 24 f 1°C except the Grand Beach, Manitoba and the Loveland, Colorado populations, which were held at light-dark 12:12, 24 k 1°C. Because of low numbers, the Saltillo population was not included.
JAMESR. NECHOL~et al.
630
diapause-inducing photoperiods terminated diapause spontaneously, i.e. with no apparent stimulus, and pupated within 70 to 130 days after spinning (Tables 3, 4). The diapause-inducing and diapausemaintaining photoperiod had no significant effect on the duration of diapause Fable 31. Diapause duration had a significant positive relationship with the latitudinal origin of the populations (Fig. 1). Northern populations remained in diapause longer than did southern populations. Although both the critical photoperiod and diapause duration were significantly related to latitude, there was no significant correlation between the two values. * Post -diapause development
170
I
30
35
45
oNORTH
50
LATITUDE
Fig. 1. Relationship between latitude and diapause responses in geographical populations of Chrysopa oculata. The relationship between latitude and the &i&al photoperiod is positive and significant (R* = 0.65; P < 0.003); the relationship between latitude and diapause duration is also positive and significant (R’ = 0.61; P < 0.02).
of the regression presented in the Appendix.
y-intercept
curves.
The curves are
RESULTS Critical photoperiod for diapause induction
The critical photoperiods of the ten geographical populations had a highly significant positive relationship with the latitudinal origin of the populations (Fig. 1). The northern-most populations (Grand Beach, Manitoba and Brownstown, Washington) had critical photoperiods over light-dark 14: 10, whereas the critical photoperiods of the southern-most populations (Quincy, Florida, and Saltillo, Coahuila), ranged between lightdark 12.5:ll.S and light-dark 11.5:12.5 (Table 2). All individuals from each population, except the one from Saltillo, Coahuila, entered diapause uniformly in response to daylengths below the critical photoperiod (Table 2). In the Saltillo population, even the shortest daylength we tested (light-dark 10: 14) induced diapause in only 50% of the individuals tested. Diapause duration
Diapausing individuals that were maintained under *Product-Moment Correlation Coefficient (Sokal and Rohlf, 1981), rlz =0.605, u = 5, P > 0.05. R2 = 0.02, tTota1 post-diapause development--t: P < 0.34;-K: R* = 0.12, P < 0.24; Prepupa--t: R* = 0.29, P < 0.21;-K: R* = 0.60, P i 0.03; Pupa-r: R2= -0.10, P<0.54;-K: R2= -0.19, P
The rate of post-diapause development in all populations tested was directly related to temperature. Thermal thresholds (t) for total post-diapause development ranged from 9.2 to 12.2”C, and day-degree requirements (K) ranged from 228 to 351”D (Table 4; see Appendix 1 for stage-specific data). Interpopulation variation was relatively high, but there was no clear geographical pattern to the interpopulation differences in the post-diapause developmental times. Both t and K were generally not well correlated with the latitudinal origin of the populations. Of all the parameters we tested only prepupal K was significantly related to latitude?. Analysis of covariance showed some significant interpopulation differences in the rates of development and in the thresholds (i.e. the slopes and y intercepts of the regression curves). However, the pattern of variation was variable and showed no consistent relationship with latitude. There was a highly significant, negative correlation between the slopes and y intercepts for total post-diapause development, as well as for post-diapause prepupal and pupal development$ . post-diapause males In general, emerged significantly earlier than females (t-test; P = 0.05), and the degree of difference between the sexes was related to temperature. For example, under 15.6”C, males emerged from 4 to 9 days earlier than females; at 26.7”C the difference ranged from 0.5 to 1 day. DISCUSSION
The various ecophysiological responses that regulate C. oculata’s seasonal cycle differ in the degree to which they are related to geographical gradients. Of the traits we studied, the critical photoperiod for diapause induction is most highly correlated with the latitudinal origin of the population. There is a strong north-south cline in photoperiodic responses-with diapause induction in northern populations occuring under longer daylengths (shorter nightlengths) than in southern populations. Such a pattern of variation in the critical photoperiod for diapause induction is typical of many “long-day” species (Danilevskii, 1965; Beck, 1980; Tauber et al., 1986). It suggests that considerable genetic variability underlies this trait and that this variability is affected by natural selection. Besides latitude, altitude may modify the critical photoperiod. For example, in the pitcher-plant mos-
Geographical variability quito, Wyeomyia smithii, latitude accounts for 80.5% of the variation in the critical photoperiod for diapause maintainance; altitude accounts for an additional 15.5% (Bradshaw, 1976). Although variation in C. oculata’s critical photoperiod for diapause induction may be similarly affected by altitude, our study did not address this problem because of lack of samples from a range of altitudes across a single latitude. Like the timing of diapause induction, diapause duration can be a very important factor in synchronizing insect life cycles with seasonal conditions (Tauber et al., 1986). For example, geographical variation in the length of diapause is a critical factor maintaining univoltinism throughout the extensive latitudinal range of the cricket, Teleogryllus emma (Masaki, 1967, 1978a). The duration of diapause in C. oculata is also positively related to latitude (Fig. 1). However, the adaptive value, if any, of this relationship is unknown. Diapause ends spontaneously during early to mid-winter in C. oculata, and the timing of vernal emergence is determined primarily by the post-diapause thermal responses, not by the duration of diapause. Thus, it is not clear why diapause is less persistent in southern than in northem C. oculata populations. A parallel, similarly unexplained situation exists in another multivoltine chrysopid, Chrysoperla carnea (Tauber and Tauber, 1982). Another aspect of dormancy in C. oculata that varies with the latitudinal origin of the population is the incidence of diapause under short daylengths. In the populations from Canada and the United States, all individuals entered diapause when they were exposed to daylengths below the critical photoperiod (Table 2). However, only 50% of larvae from the southern-most population (Saltillo, Coahuila) entered diapause under the shortest daylength we tested (light-dark 10: 14). This daylength is slightly shorter than the shortest day of the year (sunrise to sunset) at the latitude of Saltillo (Beck 1980). Low temperatures enhance the diapause-inducing effects of short daylengths in C. oculata (Tauber et al., 1987), so we presume most individuals in the Saltillo population enter diapause under the cool, short days of autumn (Tauber et al., 1987). These findings are consistent with the general pattern of latitudinal variation in the importance of photoperiod to insect diapause. Low latitudes experience smaller seasonal changes in daylength than do high latitudes. Thus, it is not unexpected that nonphotoperiodic stimuli (e.g. temperature, humidity, food quality or quantity) play a relatively large role in diapause induction among insects from low latitudes (Tauber et al., 1986). The duration of the post-diapause period in C. oculata, which we define as the time from diapause termination until adult emergence, is largely temperature dependent. After diapause ends, pupal development begins when temperatures exceed the lower threshold, t; the rate of development is determined by the slope of the line, K = y(d - t), where y = mean developmental time in days and d = temperature. Thus, two ecophysiological traits are involved in the determination of post-diapause development; the threshold for the initiation of devel-
631
opment and the thermal requirements for development above this threshold. Our data provide little evidence for interpopulation (latitudinal) variation in the post-diapause t and K values. If there are differences among C. oculata populations, the intrapopulation variation is too great to give it significance. In general, absence of latitudinally correlated patterns of variability, such as we found for the thermal regulation of post-diapause development, reflects one or a combination of causes: (a) low genetic variability in the trait, (b) physiologically or genetically mediated constraints on the expression of variation in the trait, (c) predominance of non-geographical selection pressure on the trait, or (d) the unimportance of the trait to fitness. On the basis of our findings we conclude that the post-diapause thermal responses of C. oculata have substantial variability, at least within populations. This variation probably has very important ecological significance. If temperatures hover around the threshold, as they commonly do in mid- to late spring, a degree’s difference in threshold values can amount to differences of many days in emergence time (e.g. Tauber and Tauber, 1976). The physiological and genetic bases for the variability in post-diapause development are open to analysis, as are the genetic and functional relationships between the physiological mechanisms that determine the thermal requirements for development. Analyses of the variability in the temperature/development rate curves may be of considerable significance in studying these problems. Our data show a very strong, negative correlation between the slopes and the Y-intercepts of the curves. This pattern of correlation applies both to non-diapause as well as post-diapause development (Tauber et al., 1987). It suggests that there may be physiological and/or genetic correlations between the lower thermal threshold for development and the thermal requirements for development above this threshold. Such a correlation of traits may have an important role in determining the extent and rate of the evolution of developmental responses to temperature. Acknowledgements-We thank R. G. Helgesen and D. C. Margolies, Kansas State University, for their thoughtful comments on the manuscript. We acknowledge the following people for their cooperation in collecting specimens: G. F. Tamaki (deceased),.U.S.D.A., Yakima; w.-H. Whitcomb. Universitv of Florida. Gainesville; G. W. Frankie and J: A. Poweli, Universtiy bf California, Berkeley; G. L. Godfrey, Illinois Natural History Survey, Urbana; P. J. Tauber. M. J. Tauber. A. J. Tauber. and B. D. Nechols. We also acknowledge the help of J. Higgins and J. Boyer, Kansas State University, and G. Casella, Cornell University, for advice on the statistical analysis. This work was supported, in part, by National Science Foundation grants no. DEB-7725486 and DEB-8020988.
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632
JAMES R. NECHOLS et al.
Danilevskii A. S. (1965) Photoperiodism and Seasonal Development of Insects. Oliver and Boyd, Edinburgh. Dingle H., Alden B. M., Blakley N. R., Kopec D. and Miller E. R. (1980a) Variation in photoperiodic response within and among species of milkweed bugs (Oncopeltus). Euolution 34, 356370. Dingle H., Blakley N. R. and Miller E. R. (1980b) Variation in body size and flight performance in milkweed bugs (Oncopeltus). Evolution 34, 371-385.
Hegmann J. P. and Dingie H. (1982) Phenotypic and genetic covariance structure in milkweed bug life history traits. In Evolution and Genetics of Life Histories (Ed. by Dingle H. and Hegmann J. P.), pp. 177-185. Springer, New York. Holzapfel C. M. and Bradshaw W. E. (1981) Geography of larval dormancy in the tree-hole mosquito, Aedes friseriatus (Say). Can. J. Zoo/. 59, 10141021. Istock C. A. (1978) Fitness variation in a natural population. In Evolution of Insect Migration and Diapause (Ed. by Dingle H.), pp. 171-190. Springer, New York. Istock C. A. (1981) Natural selection and life history variation: theory plus lessons from a mosquito. In Insect Life History Patterns (Ed. by Denno R. F. and Dingle H.), pp. 113-127. Springer, New York. Kidokoro T. and Masaki S. (1978) Photoperiodic response in relation to variable voltinism in the ground cricket, Pteronemobius fmcipes Walker (Orthoptera: Gryllidae). Jap. J. Ecol. 28, 291-298.
Masaki S. (1967) Geographical variation and climatic adaptation in a field cricket (Orthoptera: Gryllidae). Evolution 21, 725-741.
Masaki S. (1978a) Seasonal and latitudinal adaptations in life cycles of crickets. In Evolution of Insect Migration and Diapuuse (Ed. by Dingle H.), pp. 72-100. Springer, New York. Masaki S. (1978b) Climatic adaptation and species status in the lawn ground cricket. II. Body size. Oecologia 35, 343-356. Masaki S. (1979) Climatic adaptation and species status in the lawn ground cricket. I. Photoperiodic response. Kontyli 41, 4865.
Propp G. D., Tauber M. J. and Tauher C. A. (1969) Diapause in the neuropteran Chrysopa oculata. J. Insect Physiot. 15, 17491757. SAS User’s Guide: Statistics (1982) SAS Institute, Inc.. Cary, North Carolina. Sokal R. R. and Rohlf F. J. (1981) Biomerry, 2nd edn. W. H. Freeman and Co., San Francisco. Tauter M. J. and Tauber C. A. (1976) Environmental control of univoltinism and its evolution in an insect species. Can. J. Zool. 54, 260-266. Tauber C. A. and Tauber M. J. (1982) Evolution of seasonal adaptations and life history traits in Chrysopa: response to diverse selective pressures. In Euolufion and Genetics of Li,& Histories (Ed. by Dingle H. and Hegmann J. P.), pp. 51-72. Springer, New York. Tauber C. A. and Tauber M. J. (1986) Ecophysiological responses in life-history evolution: evidence for their importance in a geographically widespread insect speciescomplex. Can. J. Zool. 64, 875-884. Tauber M. J., Tauber C. A. and Masaki S. (1986) Seasonal Aduptations of Insects. Oxford University Press, New York. Tauber C. A., Tauber M. J. and Nechols J. R. (1987) Thermal requirements for development in Chrysopa oculafa: a geographically stable trait. Ecology. In press. Taylor F. (1981) Ecology and evolution of physiological time in insects. Am. Nat. 117, l-23.
Beach,
Florida
Quincy,
Texas
(6) 51.4k3.2cd (10) 50.3 f 3.6 cde (10) 56.9 f 3.7 b (18) 48.2 + 4.9 de (10)
69.8 f 8.2 a (19) 46.9 + 3.6 e (34) 52.8 + 4.0 c
35.0 + 1.7 a (21) 25.2f2.1e (33) 28.1 f 2.0 (6) 28.8 k 2.0 cd (11) 28.4 + 1.5 d (10) 32.3 + 1.2 b (18) 29.9 f 2.3 c (10)
(15) 25.8 + 1.9 b (21) 26.8* 1.9b (17) different
(14) 20.4 +_0.5 bc
(16) 30.2+ 1.9a
(14) 36.1 k 7.0~ (15) 38.5 f 2.4 bc (19) 39.7 f 4.0 b (13) at P = 0.05 (Duncan’s
(21) 20.1 f 1.1 c (15)
(13) 21.4*0.8b
(14) 26.6 f 3.2 b
(53) 26.5 f 2.0 b
(55) 42.2 + 3.8 a (10) 39.7 f 2.1 b
(36) 24.0& 1.9~
12.0* l.Oab (41) 11.4*0.7be (56) 11.3* 1.3c (10) 11.9* l.Oab (13) 12.5 + 0.5 a (14) 12.2 k 0.7 a (21) 12.1 +_ 1.0 a (15)
25.3 + 2.9 a (40) 19.8_+ 1.0~ (56) 19.6 f 0.7 c (10) 19.9 + 1.0 c
29.5 f 3.3 a
(36) 32.8* 1.9d
Total
(17)
(19) 16.3 +_ 1.4 b
c
a
c
38.6 f 3.8 bc
(14) 23.6 f 1.1 a (15) 22.3 + 0.9 b (20) 23.4 +_ 1.6 a (12)
(10) 22.8 + 1.2 ab
c
(54) 14.9 f 0.8 (14) 14.8 k 0.7 (16) 18.3 f 1.3 (15) 14.5 f 0.9
(55) 23.4+ 1.6a
1.0 b
(39) 13.6+ 1.2d
(37) 19.1 f 0.9 c
PuPa 15.6*
19.4 * 1.5 c
*See Table 1 for full locality data. tValues within columns followed by same letter are not significantly
Station,
College
Colorado
Loveland,
Utah
N.M.,
New York
Washington
Manitoba
Texas
Dinosaur
Ithaca,
Brownstown,
Beach,
Florida
Quincy,
Grand
Station,
Colorado
Loveland,
College
N.M.,
Dinosaur
Utah
New York
Washington
Manitoba
Ithaca,
Brownstown,
Grand
Multiple
(14) 15.1 +0.6ab (21) 14.7 f 0.8 b (15)
(12) 15.4 f 0.7 a
(13) 14.8 f 0.9 b
(56) 15.5 f 0.4 a
14.7 f 1.1 b
(14) 8.5 f 0.5 a (21) 8.4+_0.5a (15)
(56) 8.5 f 0.9 a (15) 8.5 +0.5 a (12) 8.6 f 0.5 a
8.6 + 0.9 a
Range
Test).
[y-= 0.0030x 11.4 * 1.4 [y = 0.0038x ll.Of2.7 [y = 0.0036x
9.9 f 4.6 [ y = 0.0029x 9.8 k 1.8 [y = 0.0035x 12.2 f 2.2 [y =0.0041x 11.3k2.4 9,2v;3y80038x
352.3 f - 0.02771 275.5 k - 0.03371 227.6 f -0.0480] 253.1 f - 0.04241 332.1 f - 0.02751 253.1 + - 0.04261 260.8 + - 0.03831
34
13
51
26
32
12
45
162.2 f 14.4 10.6 + 3.2 [y = 0.0062x - 0.0649] 161.0 f 12.8 9.5 + 3.3 [ y = 0.0060x- 0.0544] 12.5 f 2.8 120.3 + 11.6 [y =0.0081x -O.lOlO] 161.2 + 12.5 10.5 +_ 2.5 [y = 0.0062x - 0.0653] 178.6 + 45.6 10.2 f 4.8 [ y = 0.0054x - 0.05481 11.1 k2.7 151.2 + 14.6 [y =0.0063x - 0.0685] ll.Ok2.3 157.5 f 16.0 [y = 0.0061x - 0.0658]
Copyright 0
C022-1910/87 $3.00 +O.OO 1987 Pergamon Journals Ltd
GEOGRAPHICAL VARIABILITY IN ECOPHYSIOLOGICAL TRAITS CONTROLLING DORMANCY IN CHRYSOPA OCULATA (NEUROPTERA: CHRYSOPIDAE) JAMESR. NECHOLS’, MAURICEJ. TAUBER~ and CATHERINE A. TAUBER~ *Department of Entomology, Kansas State University, Manhattan, KS 66506 and TDepartment of Entomology, Comstock Hall, Cornell University, Ithaca, NY 14853-0999, U.S.A. (Received 22 July 86; revised 6 January 1987)
Abstract-Dormancy in Chrysopa oculata, a multivoltine species, is controlled by reponses to photopcriod and temperature. Variation in both the critical photoperiod for diapause induction and the duration of diapause is positively related to the latitudinal origin of the population. The incidence of photoperiodically induced diapause also varies geographically; at 24°C the southern-most population is more variable for diapause induction than the northern populations. By contrast, there is little interpopulation variation in thermally determined rates of post-diapause development. The results suggest that the lower threshold for development and the thermal requirements above the threshold may be functionally correlated. Key Word Index: Diapause, photoperiod,
geographical variation, thermal responses, Chrysopa
INTRODt_JCTION While undergoing dormancy, insects progress through a series of distinct physiological phasesdiapause induction, maintenance and termination, post-diapause quiescence, and post-diapause development. Each of these phases is characterized by a set of ecophysiological responses which appear to evolve in a coordinated manner to adapt insects to the seasonally variable physical and biotic conditions of their local environment (see Tauber et al., 1986). Therefore, knowledge of the genetic variation and adaptive significance of the response patterns expands the understanding of the physiology of dormancy. In theory, all of the response patterns that control dormancy should be subject to equivalent evolutionary modification over space and time. But, in reality, some appear to exhibit much greater variation than others. For example, among geographically widespread insect species, the photoperiodic induction of diapause is generally highly variable, whereas the species-specific diapausing stage and the thermal regulation of developmental and reproductive rates are relatively conservative in their variation (Danilevskii, 1965; Taylor, 1981; Tauber et al., 1986). This biased pattern of intraspecific variability raises the question of how ecophysiological responses interact with each other. Do the various responses vary independently or are they genetically or functionally correlated? Are some traits innately more variable than others? Do genetic correlations (e.g. linkage) between physiological traits set limits to the expression of variation among the traits? Resolution of these questions is necessary for understanding how the physiological adaptations underlying dormancy
evolve-the rates of their evolution, the limits to their evolution, etc. Numerous studies with insects have examined variability in a single seasonal response pattern-the critical photoperiod for diapause induction being the most common (see Tauber et al., 1986). However, very few have examined variation in sets of seasonal responses (e.g. Istock 1978, 1981; Kidokoro and Masaki, 1978; Masaki, 1978a, b, 1979; Dingle et al., 1980a, b; Holzapfel and Bradshaw, 1981; Hegmann and Dingle, 1982; Tauber and Tauber, 1982, 1986). Thus, to initiate a study of the relationship among seasonally important ecophysiological traits, we investigated the pattern of geographical variability in a suite of responses that control dormancy from its onset through its termination in a widespread North American species of insect predators. We examined various aspects of diapause and post-diapause development: specifically the photoperiodic induction of diapause, the innate duration of diapause, the photoperiodic influence on diapause duration, and the thermal regulation of postdiapause development. MATERIALSAND METHODS Experimental animal Chrysopa oculata Say is multivoltine throughout its range, which comprises all of the contiguous United States, southern Canada, and parts of northern Mexico. Adults emerge in the spring; reproduction and development take place throughout the summer and autumn until frosts occur (Tauber et al., 1987). Both adults and larvae are predaceous, so the initiation of oviposition and the timing of the summer generations depend on temperature and the availability of prey (Tauber et al., 1987). 627
JAMESR. NECHOLS et al.
628
Table I. Localitv data for neoaranhical Domdations of Chryso~a oculalo tested in this studv Locality
Latitude
Grand Beach, Lake Winnipeg, Manitoba, Canada Brownstown, 15 mi. SW Yakima, Yakima Co., Washington Ithaca, Tompkins Co., New York Dinosaur National Monument (Green River Campgrd.), Uintah Co., Utah IOmi. W. Loveland, Larimer Co., Colorado Manhattan, Riley Co., Kansas Lubbock, Lubbock Co., Texas College Station, Brazes Co., Texas Quincy, Gadsden Co., Florida 17mi. SE Saltillo. Coahuila, Mexico
50”34’ N 46”31’ N 42”26’ N 40”27’ N 40”24’ N 39”ll’N 33”35’ N 30”38’ N 30”34’ N 25”30’ N
C. ocufata overwinters as mature, diapausing thirdinstar larvae (“prepupae”) within cocoons. Diapause is induced primarily by photoperiod; exposure of second and third-instar larvae to short daylengths/ long nightlengths induces diapause (Propp et al., 1969). Thus, C. oculata is a “long-day species” (Type 1 of Beck 1980). As is typical of most long-day species, low temperatures enhance the diapauseinducing effects of photoperiod (Tauber et al., unpublished). Thus, if summer temperatures are low, diapause is induced earlier than if conditions remain warm. Once induced, diapause persists under short daylengths in the laboratory for about 3-4 months. Subsequently, it terminates spontaneously, i.e. apparently without external stimulus. Exposure to cold is not necessary for diapause termination or the successful completion of post-diapause development in this species (Propp et al., 1969). Postdiapause development comprises two stages: the prepupal stage which extends from diapause termination by the third-instar larvae to the larval-pupal moult, and the pupal stage which lasts from the larval-pupal moult to adult emergence. Experimental procedures
Adults of C. oculata were collected at numerous localities throughout the range of the species (Table 1). The number of fertile females collected was greater than ten for each population except three (Dinosaur National Monument, Utah, Loveland, Colorado, Saltillo, Coahuila), each of which had three mated females. All tests were run with first-generation offspring of field-collected adults. Be-
Elevation (ft) 764 1066 815 -8000 _ 5000 1066 3240 308 187 6800
cause they are cannibalistic, larvae were reared in individual shell vials. The larval diet consisted of pea aphids, Acyrthosiphon pisum (Harris). Adults were provided pea aphids and a proteinaceous diet (a 1: 1: 1: 1 volumetric mixture of Wheast@, protein hydrolysate of yeast, sugar and honey). At 24”C, nondiapause individuals pupate within 10 days of spinning. Thus, we considered individuals that did not pupate within this period to be in diapause. In almost all cases, diapausing larvae did not pupate until they had been in the cocoon for 70 days. To examine the variability in photoperiodic induction of diapause among the ten geographical populations, we reared individuals from each population under a range of constant photoperiods from light-dark 10: 14 to light-dark 16:8 (Temperature = 24 f 1’C) (Table 2). We recorded the incidence of delayed pupation under each condition and used these data to determine the critical photoperiod. For all populations except Saltillo, we followed standard procedures and designated the critical photoperiod as the photoperiod at which 50% of the larvae entered diapause. Because even under the shortest daylengths tested, only a proportion of Saltillo individuals entered diapause, we used the midpoint between the maximal and minimal response as the critical photoperiod for this population. This value represents 50% of the individuals that are susceptible to diapause induction under our laboratory conditions (24 + l”C, surplus of food). To determine the variability in the length of diapause and to examine the relationship between the critical photoperiod and diapause duration, we main-
Table 2. Geographical variation in photoperiodic induction of diapause among North American populations of Chrvsooo oculata (Temo = 24 + 1°C) IO Geographical
population*
Grand Beach, Manitoba Brownstown, Washington Ithaca, New York Dinosaur Nat]. Mon., Utah Loveland, Colorado Manhattan, Kansas Lubbock, Texas College Station, Texas Quincy, Florida Saltillo. Coahuila
Daylength per 24 hours 12 13
II
14
IS
16
% Diapause (No. individuals)
-
100(49) 100(25) lOO(57) lOO(12) 1OO(24) lOO(l2) lOO(12) 50(8)
loo(l6) loo(ll) 33I6)
WW W22) loo(62) loO(16) 86(l4) loo(38) loo(l2) 10009) 92(12) o(8)
lC$) 36(44) lOO(20) 93(15) 13(38) 27(11) 80(20) 36(11) o(8)
65(11) 90(20) o(63) 25(24) lo(l0) o(37) 002) o(l8) o(l2) M8)
*See Table 1 for full locality data. Two other photoperiods were tested for the Ithaca, New York, population: light-.iark (36); light-dark 13.5: 10.5 = 3% (37).
‘X18) WV O(43)
ow
O&l, 005) -
:$z; O(37)
O(39)
00
12.5: 1I .5 = 100%
Geographical variability
629
Table 3. Relationship between diapause-inducing/-maintaining photoperiod and diapause duration (time to pupation, which includes a short period of post-diapause development) in North American populations of Chrysopa oeulara (Temp. = 24 + 1°C) Duration of diapause P + SD days (No.) Geographical
10: 14
population*
Grand Beach, Manitoba Brownstown, Washington Dinosaur, NM., Utah Loveland, Colorado College Station, Texas Quincy, Florida
11:13 -
125 + 23abt (49) 91 f 25a (44) -
-
72 + 2Oab (12) 84 * 27a (10)
83 rt 12a (16) 85 k 9a (9)
Photoperiod light-dark 12: I2 106 k 23at (18) 112+ 16b (20) 77 5 24a (16) 82+ 16b (12) 65 k 17b (20) 66 * 29a (11)
13:ll
131 + 28a (20) 96+4la 08) 103 + 19a (13) 74k llab (16) 61 + 15a (3)
14:lO 103 f 30a (11) 139k28a (17) 94i lla (5) -
*See Table 1 for complete locality data. tValues within rows followed by same letter are not significantly different at P = 0.05 [f-test (LSD)].
tained diapausing individuals under their diapauseinducing daylengths until pupation (Table 3). Every day for 2 weeks after spinning, cocoons were checked for pupation; subsequently, they were examined every third day. The larval-pupal ecdysis was used as an indicator that diapause had ended; thus our estimates of diapause duration (Tables 3 and 4) include an 8 to IO-day period of post-diapause development. To compare thermal requirements for postdiapause development among the geographical populations, we reared individuals from seven localities under short-day conditions (lightdark 10: 14, 24 + 1’C) to induce diapause. Three weeks after the larvae had spun cocoons, we transferred them from 24 to 4 + 1°C (light-dark 10: 14), where they were held untidiapause ended-approximately 4 months. Subsequently, we divided the cocoons among five conditions consisting of a range of temperatures from 15.6 to 24°C (all f 1”) under light-dark 16 : 8 and 24°C under light-dark 10: 14 (Table 4; Appendix 1). Each condition was replicated three times. Developmental times (in days) were recorded for the two post-diapause stages (the prepupal stage-from the day of transfer until larval-pupal ecdysis, and the
pupal stage-from larval-pupal ecdysis to adult emergence). The individuals under short daylengths served to determine if diapause had ended by the time the cocoons were transferred to the temperature conditions. In the six populations tested, photoperiod had no significant effect on the time to pupation after cocoons were transferred from the cold to a development-favouring temperature [24 + l“C] (t-test; P = 0.05). Thus, diapause had ended before we began our tests on post-diapause development. In analyzing the relationship between temperature and development, we computed the reciprocal of the development times (y-axis) at every temperature (x-axis for individuals from each strain and then fitted these data to linear regression curves using the least squares method. We estimated the lower thermal threshold for development, t, by linear extrapolation through the x-axis (temperature), and we derived the thermal constant, K, by the equation K = y(d - t), where y = mean developmental time in days and d = temperature (“C). We used the analysis of covariance procedure (SAS Institute 1982) to test for interpopulation differences in the slope and the
Table 4. Geographical variation in diapause duration (time to pupation, which includes a short period of postdiapause development) and in the thermal requirements (I and K) for postdiapause development among North American populations of Chrysopo oculara (see Appendix for stage-specific data)
Geographical
population*
Grand Beach, Manitoba Brownstown, Washington Ithaca. New York Dinosaur Nat]. Mon., Utah Loveland, Colorado College Station, Texas Quincy, Florida
Duration of diapause X f SD days (No.)t 106 & 23(18)b 125 + 23(49)a 93 f 1l(33)c 91 f 25(44)c 82 + 16(12)cd 72 f 20(12)d 80 f 18(37)cd
Thermal requirements for post-diapause development r(C + SE) K(D-D&SE) 9.9 +_4.6 9.8 k 1.8 12.2 f 2.2 11.322.4 9.2 i 3.8 11.4* 1.4 ll.Ok2.7
351 + 45 276112 228 f 32 253 f 26 332 f 51 253 k 13 261 & 34
*See Table I for complete locality data. tValues followed by same letters are not significantly different at P = 0.05 (Duncans’s Multiple Range Test). All populations were maintained under light-dark 10: 14; 24 f 1°C except the Grand Beach, Manitoba and the Loveland, Colorado populations, which were held at light-dark 12:12, 24 k 1°C. Because of low numbers, the Saltillo population was not included.
JAMESR. NECHOL~et al.
630
diapause-inducing photoperiods terminated diapause spontaneously, i.e. with no apparent stimulus, and pupated within 70 to 130 days after spinning (Tables 3, 4). The diapause-inducing and diapausemaintaining photoperiod had no significant effect on the duration of diapause Fable 31. Diapause duration had a significant positive relationship with the latitudinal origin of the populations (Fig. 1). Northern populations remained in diapause longer than did southern populations. Although both the critical photoperiod and diapause duration were significantly related to latitude, there was no significant correlation between the two values. * Post -diapause development
170
I
30
35
45
oNORTH
50
LATITUDE
Fig. 1. Relationship between latitude and diapause responses in geographical populations of Chrysopa oculata. The relationship between latitude and the &i&al photoperiod is positive and significant (R* = 0.65; P < 0.003); the relationship between latitude and diapause duration is also positive and significant (R’ = 0.61; P < 0.02).
of the regression presented in the Appendix.
y-intercept
curves.
The curves are
RESULTS Critical photoperiod for diapause induction
The critical photoperiods of the ten geographical populations had a highly significant positive relationship with the latitudinal origin of the populations (Fig. 1). The northern-most populations (Grand Beach, Manitoba and Brownstown, Washington) had critical photoperiods over light-dark 14: 10, whereas the critical photoperiods of the southern-most populations (Quincy, Florida, and Saltillo, Coahuila), ranged between lightdark 12.5:ll.S and light-dark 11.5:12.5 (Table 2). All individuals from each population, except the one from Saltillo, Coahuila, entered diapause uniformly in response to daylengths below the critical photoperiod (Table 2). In the Saltillo population, even the shortest daylength we tested (light-dark 10: 14) induced diapause in only 50% of the individuals tested. Diapause duration
Diapausing individuals that were maintained under *Product-Moment Correlation Coefficient (Sokal and Rohlf, 1981), rlz =0.605, u = 5, P > 0.05. R2 = 0.02, tTota1 post-diapause development--t: P < 0.34;-K: R* = 0.12, P < 0.24; Prepupa--t: R* = 0.29, P < 0.21;-K: R* = 0.60, P i 0.03; Pupa-r: R2= -0.10, P<0.54;-K: R2= -0.19, P
The rate of post-diapause development in all populations tested was directly related to temperature. Thermal thresholds (t) for total post-diapause development ranged from 9.2 to 12.2”C, and day-degree requirements (K) ranged from 228 to 351”D (Table 4; see Appendix 1 for stage-specific data). Interpopulation variation was relatively high, but there was no clear geographical pattern to the interpopulation differences in the post-diapause developmental times. Both t and K were generally not well correlated with the latitudinal origin of the populations. Of all the parameters we tested only prepupal K was significantly related to latitude?. Analysis of covariance showed some significant interpopulation differences in the rates of development and in the thresholds (i.e. the slopes and y intercepts of the regression curves). However, the pattern of variation was variable and showed no consistent relationship with latitude. There was a highly significant, negative correlation between the slopes and y intercepts for total post-diapause development, as well as for post-diapause prepupal and pupal development$ . post-diapause males In general, emerged significantly earlier than females (t-test; P = 0.05), and the degree of difference between the sexes was related to temperature. For example, under 15.6”C, males emerged from 4 to 9 days earlier than females; at 26.7”C the difference ranged from 0.5 to 1 day. DISCUSSION
The various ecophysiological responses that regulate C. oculata’s seasonal cycle differ in the degree to which they are related to geographical gradients. Of the traits we studied, the critical photoperiod for diapause induction is most highly correlated with the latitudinal origin of the population. There is a strong north-south cline in photoperiodic responses-with diapause induction in northern populations occuring under longer daylengths (shorter nightlengths) than in southern populations. Such a pattern of variation in the critical photoperiod for diapause induction is typical of many “long-day” species (Danilevskii, 1965; Beck, 1980; Tauber et al., 1986). It suggests that considerable genetic variability underlies this trait and that this variability is affected by natural selection. Besides latitude, altitude may modify the critical photoperiod. For example, in the pitcher-plant mos-
Geographical variability quito, Wyeomyia smithii, latitude accounts for 80.5% of the variation in the critical photoperiod for diapause maintainance; altitude accounts for an additional 15.5% (Bradshaw, 1976). Although variation in C. oculata’s critical photoperiod for diapause induction may be similarly affected by altitude, our study did not address this problem because of lack of samples from a range of altitudes across a single latitude. Like the timing of diapause induction, diapause duration can be a very important factor in synchronizing insect life cycles with seasonal conditions (Tauber et al., 1986). For example, geographical variation in the length of diapause is a critical factor maintaining univoltinism throughout the extensive latitudinal range of the cricket, Teleogryllus emma (Masaki, 1967, 1978a). The duration of diapause in C. oculata is also positively related to latitude (Fig. 1). However, the adaptive value, if any, of this relationship is unknown. Diapause ends spontaneously during early to mid-winter in C. oculata, and the timing of vernal emergence is determined primarily by the post-diapause thermal responses, not by the duration of diapause. Thus, it is not clear why diapause is less persistent in southern than in northem C. oculata populations. A parallel, similarly unexplained situation exists in another multivoltine chrysopid, Chrysoperla carnea (Tauber and Tauber, 1982). Another aspect of dormancy in C. oculata that varies with the latitudinal origin of the population is the incidence of diapause under short daylengths. In the populations from Canada and the United States, all individuals entered diapause when they were exposed to daylengths below the critical photoperiod (Table 2). However, only 50% of larvae from the southern-most population (Saltillo, Coahuila) entered diapause under the shortest daylength we tested (light-dark 10: 14). This daylength is slightly shorter than the shortest day of the year (sunrise to sunset) at the latitude of Saltillo (Beck 1980). Low temperatures enhance the diapause-inducing effects of short daylengths in C. oculata (Tauber et al., 1987), so we presume most individuals in the Saltillo population enter diapause under the cool, short days of autumn (Tauber et al., 1987). These findings are consistent with the general pattern of latitudinal variation in the importance of photoperiod to insect diapause. Low latitudes experience smaller seasonal changes in daylength than do high latitudes. Thus, it is not unexpected that nonphotoperiodic stimuli (e.g. temperature, humidity, food quality or quantity) play a relatively large role in diapause induction among insects from low latitudes (Tauber et al., 1986). The duration of the post-diapause period in C. oculata, which we define as the time from diapause termination until adult emergence, is largely temperature dependent. After diapause ends, pupal development begins when temperatures exceed the lower threshold, t; the rate of development is determined by the slope of the line, K = y(d - t), where y = mean developmental time in days and d = temperature. Thus, two ecophysiological traits are involved in the determination of post-diapause development; the threshold for the initiation of devel-
631
opment and the thermal requirements for development above this threshold. Our data provide little evidence for interpopulation (latitudinal) variation in the post-diapause t and K values. If there are differences among C. oculata populations, the intrapopulation variation is too great to give it significance. In general, absence of latitudinally correlated patterns of variability, such as we found for the thermal regulation of post-diapause development, reflects one or a combination of causes: (a) low genetic variability in the trait, (b) physiologically or genetically mediated constraints on the expression of variation in the trait, (c) predominance of non-geographical selection pressure on the trait, or (d) the unimportance of the trait to fitness. On the basis of our findings we conclude that the post-diapause thermal responses of C. oculata have substantial variability, at least within populations. This variation probably has very important ecological significance. If temperatures hover around the threshold, as they commonly do in mid- to late spring, a degree’s difference in threshold values can amount to differences of many days in emergence time (e.g. Tauber and Tauber, 1976). The physiological and genetic bases for the variability in post-diapause development are open to analysis, as are the genetic and functional relationships between the physiological mechanisms that determine the thermal requirements for development. Analyses of the variability in the temperature/development rate curves may be of considerable significance in studying these problems. Our data show a very strong, negative correlation between the slopes and the Y-intercepts of the curves. This pattern of correlation applies both to non-diapause as well as post-diapause development (Tauber et al., 1987). It suggests that there may be physiological and/or genetic correlations between the lower thermal threshold for development and the thermal requirements for development above this threshold. Such a correlation of traits may have an important role in determining the extent and rate of the evolution of developmental responses to temperature. Acknowledgements-We thank R. G. Helgesen and D. C. Margolies, Kansas State University, for their thoughtful comments on the manuscript. We acknowledge the following people for their cooperation in collecting specimens: G. F. Tamaki (deceased),.U.S.D.A., Yakima; w.-H. Whitcomb. Universitv of Florida. Gainesville; G. W. Frankie and J: A. Poweli, Universtiy bf California, Berkeley; G. L. Godfrey, Illinois Natural History Survey, Urbana; P. J. Tauber. M. J. Tauber. A. J. Tauber. and B. D. Nechols. We also acknowledge the help of J. Higgins and J. Boyer, Kansas State University, and G. Casella, Cornell University, for advice on the statistical analysis. This work was supported, in part, by National Science Foundation grants no. DEB-7725486 and DEB-8020988.
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JAMES R. NECHOLS et al.
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Propp G. D., Tauber M. J. and Tauher C. A. (1969) Diapause in the neuropteran Chrysopa oculata. J. Insect Physiot. 15, 17491757. SAS User’s Guide: Statistics (1982) SAS Institute, Inc.. Cary, North Carolina. Sokal R. R. and Rohlf F. J. (1981) Biomerry, 2nd edn. W. H. Freeman and Co., San Francisco. Tauter M. J. and Tauber C. A. (1976) Environmental control of univoltinism and its evolution in an insect species. Can. J. Zool. 54, 260-266. Tauber C. A. and Tauber M. J. (1982) Evolution of seasonal adaptations and life history traits in Chrysopa: response to diverse selective pressures. In Euolufion and Genetics of Li,& Histories (Ed. by Dingle H. and Hegmann J. P.), pp. 51-72. Springer, New York. Tauber C. A. and Tauber M. J. (1986) Ecophysiological responses in life-history evolution: evidence for their importance in a geographically widespread insect speciescomplex. Can. J. Zool. 64, 875-884. Tauber M. J., Tauber C. A. and Masaki S. (1986) Seasonal Aduptations of Insects. Oxford University Press, New York. Tauber C. A., Tauber M. J. and Nechols J. R. (1987) Thermal requirements for development in Chrysopa oculafa: a geographically stable trait. Ecology. In press. Taylor F. (1981) Ecology and evolution of physiological time in insects. Am. Nat. 117, l-23.
Beach,
Florida
Quincy,
Texas
(6) 51.4k3.2cd (10) 50.3 f 3.6 cde (10) 56.9 f 3.7 b (18) 48.2 + 4.9 de (10)
69.8 f 8.2 a (19) 46.9 + 3.6 e (34) 52.8 + 4.0 c
35.0 + 1.7 a (21) 25.2f2.1e (33) 28.1 f 2.0 (6) 28.8 k 2.0 cd (11) 28.4 + 1.5 d (10) 32.3 + 1.2 b (18) 29.9 f 2.3 c (10)
(15) 25.8 + 1.9 b (21) 26.8* 1.9b (17) different
(14) 20.4 +_0.5 bc
(16) 30.2+ 1.9a
(14) 36.1 k 7.0~ (15) 38.5 f 2.4 bc (19) 39.7 f 4.0 b (13) at P = 0.05 (Duncan’s
(21) 20.1 f 1.1 c (15)
(13) 21.4*0.8b
(14) 26.6 f 3.2 b
(53) 26.5 f 2.0 b
(55) 42.2 + 3.8 a (10) 39.7 f 2.1 b
(36) 24.0& 1.9~
12.0* l.Oab (41) 11.4*0.7be (56) 11.3* 1.3c (10) 11.9* l.Oab (13) 12.5 + 0.5 a (14) 12.2 k 0.7 a (21) 12.1 +_ 1.0 a (15)
25.3 + 2.9 a (40) 19.8_+ 1.0~ (56) 19.6 f 0.7 c (10) 19.9 + 1.0 c
29.5 f 3.3 a
(36) 32.8* 1.9d
Total
(17)
(19) 16.3 +_ 1.4 b
c
a
c
38.6 f 3.8 bc
(14) 23.6 f 1.1 a (15) 22.3 + 0.9 b (20) 23.4 +_ 1.6 a (12)
(10) 22.8 + 1.2 ab
c
(54) 14.9 f 0.8 (14) 14.8 k 0.7 (16) 18.3 f 1.3 (15) 14.5 f 0.9
(55) 23.4+ 1.6a
1.0 b
(39) 13.6+ 1.2d
(37) 19.1 f 0.9 c
PuPa 15.6*
19.4 * 1.5 c
*See Table 1 for full locality data. tValues within columns followed by same letter are not significantly
Station,
College
Colorado
Loveland,
Utah
N.M.,
New York
Washington
Manitoba
Texas
Dinosaur
Ithaca,
Brownstown,
Beach,
Florida
Quincy,
Grand
Station,
Colorado
Loveland,
College
N.M.,
Dinosaur
Utah
New York
Washington
Manitoba
Ithaca,
Brownstown,
Grand
Multiple
(14) 15.1 +0.6ab (21) 14.7 f 0.8 b (15)
(12) 15.4 f 0.7 a
(13) 14.8 f 0.9 b
(56) 15.5 f 0.4 a
14.7 f 1.1 b
(14) 8.5 f 0.5 a (21) 8.4+_0.5a (15)
(56) 8.5 f 0.9 a (15) 8.5 +0.5 a (12) 8.6 f 0.5 a
8.6 + 0.9 a
Range
Test).
[y-= 0.0030x 11.4 * 1.4 [y = 0.0038x ll.Of2.7 [y = 0.0036x
9.9 f 4.6 [ y = 0.0029x 9.8 k 1.8 [y = 0.0035x 12.2 f 2.2 [y =0.0041x 11.3k2.4 9,2v;3y80038x
352.3 f - 0.02771 275.5 k - 0.03371 227.6 f -0.0480] 253.1 f - 0.04241 332.1 f - 0.02751 253.1 + - 0.04261 260.8 + - 0.03831
34
13
51
26
32
12
45
162.2 f 14.4 10.6 + 3.2 [y = 0.0062x - 0.0649] 161.0 f 12.8 9.5 + 3.3 [ y = 0.0060x- 0.0544] 12.5 f 2.8 120.3 + 11.6 [y =0.0081x -O.lOlO] 161.2 + 12.5 10.5 +_ 2.5 [y = 0.0062x - 0.0653] 178.6 + 45.6 10.2 f 4.8 [ y = 0.0054x - 0.05481 11.1 k2.7 151.2 + 14.6 [y =0.0063x - 0.0685] ll.Ok2.3 157.5 f 16.0 [y = 0.0061x - 0.0658]