Allemand, R.

Bouletreau-Merle, J.

English

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Research Articles Expenentia 45 (1989 Birkhauser Verlag. CH-4011 Basel/Switzerland Correlated responses in lines of Drosophila melanogaster selected for different oviposition behaviours R. Allemand and J. Boulc5treau-Merle (27 .- - Laboratoire de Gknetique des Populations ( UA CNR ivern:; Lyon 1.43 boulevard du 11 Novembre 1918, F-69622 Villeurbantte Cedex (Frattce) Received 31 January 1989; accepted 18 hla) 1989 Summary. D. melanoguster was subjected to selection for two c:tYerent traits of oviposition behaviour in relation to oocyte retention in ovaries, i.e. the aptitude to stop laying in response to an unsuitable substrate, and the occurrence of a dusk peak in the circadian oviposition rhythm. Selection for high and low lines was rapidly successful for both characters. Each selected line was also tested for the non-selected trait. Results showed a genetic correlation between the two behaviours, suggesting a common mechanism for the control of oviposition, independently of the origin and the duration of oocyte retention. Key words. Oviposition behavior; circadian rhythm; selection: D. melanogaster. As in other insects, egg-laying in Drosophila results from complex physiological and behavioural processes, in- volving oocyte production, ovulation and oviposition '. Egg-laying must be considered to be dependent on envi- ronmental conditions, and regulation of oviposition in- cludes intrinsic and extrinsic components2- Among ex- perimental factors that have been shown to affect the egg-laying rate, most are related to the laying substrate (humidity, components, appearence . . .3  *).  Moreover, the egg-laying pattern, in response to a photoperiodic cycle. shows circadian variations with a peak at dusk '. In all these cases, the behavioural response is expressed by an egg retention, as mature oocytes can be retained in the ovaries for several hours before deposition. independent- ly of vitellogenesis. The ability to stop egg-laying (ovipo- sition blocking) is under control of the nervous system and can occur in response to various environmental stim- uli2. The retention allows Drosophila females to find suitable oviposition sites and to deposit several eggs in a few minutes. The adaptative value of such a trait might play a major role in patchy environments. In natural populations, the existence of genetic variation for oviposition preference and oviposition time have been demonstrated '-lo. and artificial selection has been successful '+ ' '. However. only a few studies have investi- sated the genetic control of the egg-laying behaviour that - relates to the ability to block oviposition. Artificial selec- tion upon circadian oviposition rhythm and laying on an unsuitable site was therefore performed to induce reten- tion for different times, i.e. a few hours for the first trait and more than 24 h for the second one. Selected lines were analysed to determine whether selection for one oviposition trait produced any correlated changes in the other. It appeared that a common genetic system con- trols both short retention (circadian rhythm) and long retention (unsuitable substrate). Materials and methods Experiments were performed with a natural population located in Beynost, near Lyon (France). About 200 flies were caught, and from these a mass-reared population and 50 isofemale lines were founded. Strains were select- ed either for their characteristics of daily oviposition rhythm or for their oviposition blocking capacity. - Selection for oviposition blocking capacity: The term opposition blocking capacity' was used instead of egg retention to differentiate this ability to stop egg-laying (in reaction to unfavourable conditions) from the initial egg retention occurring in virgin females. The latter is due to the delay of the ovulation process at the ovariole level, whereas the former is initiated at the uterus level '. From a pool of 50 mixed isofemale lines, selection for high and low ability to stop oviposition was carried on for six generations. Females unable to stop egg-laying and fe- maks capable of long delay were mass selected in the presence of unsuitable substrate. The main trait used for selecting parents was the oviposition rate on the first day after switching the substrate. In each generation, the 6-10 most extreme females were selected out of 50 to found the next generation. - Selection for oviposition rhythm: Oviposition rhythm usually show's a broad mode during photophase and a sharp peak at dusk. Artd5cial selection attempted to de- crease the dusk peak for the low line and to increase the dusk peak for the high line. From the mass-reared popu- lation, selection was made for 9 generations. In each generation, 10 pairs were isolated and the rhythm of their offspring was recorded. The two families showing the best scores for each line were isolated. They were mixed (40 (lies) and used for the next generation out of which 10 pairs were isolated and tested. - Experiments: The four selected lines were studied for 3 or 4 generations after selection took place. Flies were reared in low density, on a killed yeast medium, under LD 12: 12 photoperiod at 25 O C .  After emergence, groups of 4 males and 4 females were transferrred into plastic boxes. Both the traits were measured on these groups between the 7th and the 12th day, when egg production is maximum and stable. Therefore, the two behaviours could not be studied on the same individuals. The substrate effect was studied by changing the com- plete, dead yeast medium for an agar + sugar medium 1148 Experientia 45 (1989). Birkhiuser Verlag. CH-4010 Basel S u ~ r l a n d  Research Articles (without flour or yeast 9, on day 10. Daily laying was recorded 3 days before and 3 da>s after the substrate had been changed. The circadian rhythm was recorded with an apparatus providing substrate to the flies continuous- ly '. with the egg position indicating the laying time. Results 1 )  Laving selection: The killed yeast medium is very suit- able for D. melanogaster oviposition. Under the experi- mental conditions used, flies from the (initial) mass- reared population laid about 60 eggs per day (table). When placed upon unsuitable agar medium, females kept the eggs in retention and oogenesis was rapidly stopped. The first day after the substrate had been changed, the laying rate was low (about 27 eggs) and no more eggs were laid after three days (total oviposition of 47 eggs, table and figure). The oviposition-blocking capacity was modified by selec- tion. The ability to retain eggs on deficient medium had shifted, producing two opposite. significantly different lines (table and figure). The realised heritabilities estimat- ed from the 6 generations were 0.18 + 0.08 for the high line and 0.31 + 0.07 for the low line. For the former, the daily fecundity was also significantly reduced (table). Rates of egg deposition on agar medium during the first day were significantly different between the two selected lines: 60 % and 20 % of the normal daily laying. Both selected lines differed also from the initial population (table and figure). The total number of eggs that were laid for 3 days on agar substrate confirms this difference despite a progressive decrease of the blocking capacity (table). 2) Rhythm selection: The oviposition rhythm of the initial population, which showed a high laying rate during pho- tophase and a peak after light-off (figure), was quite typical for populations from temperate Europe. Selection for an increased laying rate during photophase for the high line and during scotophase for the low line gave rise to modifications in the initial pattern but did not affect the daily fecundity. After 9 generations. two opposite tec2encies were observed: a rhythm with a high peak at the beginning of the scotophase and a rhythm with a low Â¥ps .^' at dusk and with a maximum laying rate during phcwphase (figure, see also Allemand et al.I0). The ef- fecx of the selection are highly significant when ex- preyed in number of eggs (table) since the night peak is enhanced by a coefficient of 4 between the two lines. The estimation of the realised heritabilities from the first 7 ger-?rations are 0.27 Â 0.09 for the high line and 0.4" + 0.06 for the low line. 3) Correlations between selections: The lines selected for one behaviour were tested for the other one. Results are presented with the previous ones on the figure and in the tabk. The daily fecundities estimated in the two kinds of experiments are similar (r = 0.94, p < 0.05). In both cas- es- the trait that had not been directly selected was signif- icantly modified and one can observe a good similarity beween high laying after substrate change and a rhythm uim a low dusk peak, and also between low laying after substrate change and a high peak. However, the correla- tion between the two traits, calculated on the lines and on the initial population. is not significant (r = 0.85, p < 0.10). The modification of the unselected trait was ahrays of less importance than modifications in lines that were specif~cally selected for this character (and was sometimes insignificant). DISLÂ¥ussio Artificial selection for oviposition behaviours can give rise to genetic divergences in D. melanogaster. Response to selection for the two behavioural traits, blocking ca- padty and daily rhythm, confirms the genetic plasticity of the oviposition behaviour which has been selected in the past for some aspects of the oviposition site prefer- ence (OSP), the choice between two media l1 or the ten- dency to insert eggs in the substrate5. Maxion for %-laying 0x1 an unsuitable substrate and for the circadian r h > e  of ovipition. Fecundit1 and laying are expressed as the number of  e g g  per female. The laying rate (%). that is recorded the first day after the d g e  of medium IS expressed as a proportion of the mean fecundity before change. n = number of groups of 4 females. Mean + standard deviation Significance of the t-tests (comparisons to the initial population and between lines):* < 0.05, ** < 0.01, ns = no significant. Egg-laying Chiposition rhythm Daily fecundity 1st day layins 3 days laying Daily fecundity Peak laving before change after chanee after change 20.00-22.00 h Initial population Laying selection Retention (high line) No retention (low tine) Rhythm selection Laying peak (high line) No laying peak (low line) Research Articles Experientia 45 (1989), Birkhguser Verlag. CH-4011 Base1,Switzerland 1149 laying selection substrate initial population + - hours 0 8 20 24 rhythm selection Selections for two oviposition behaviours: egg-laying on an unsuitable substrate and circadian rhythm of oviposition. The two behaviours are presented for the initial population and the In our experimental conditions, females are young and well fed, with a constant supply of food and of laying substrate. When they are placed on an unsuitable sub- strate, the oviposition is partially blocked and the oogen- esis is rapidly stopped, as shown by dissections. Only the few eggs that were already engaged in vitellogenesis achieved maturation and were laid during the three days after the substrates were switched. In such conditions, the laying substrate induces a strong retention which goes on for a few days. By selection, theintensity of the blocking capacity was modified. In the high line, the daily egg production was decreased, which should make the reten- tion easier. In the case of ihe circadian oviposition rhythm, the pho- toperiod induces a cyclical activity of the ovarian physi- ology. Every day, numerous synchronous oocytes com- plete vitellogenesis during the photophase and are partially retained in the ovarian tubes for the end of the photophase, till the 'light off' signal results in the laying peak. The time of retention varies between oocytes and usually does not exceed a few hours. It depends on envi- ronmental conditions such as light intensity, interactions between individuals, etc.:-13. By selection, the rhythm patterns are strongly modified without significant change selected lines. The trait that is subjected to selection is indicated with a star. (+): high line, (-): low line. in the daily egg production. For both behaviours, the response to selection estimated by the heritability values was more rapid for the low lines. in which the retention time was lowered. This difference in the response can be related to the modification of the egg production (only significant for blocking capacity) which appeared when selection attempted to increase egg retention. The two selected traits are quite different because they relate to distinctive physiological states and durations of ovarian retention. They are also different with respect to the environmental clues to which the selected flies re- sponded. The short, normal and non-obligatory reten- tion occurring in the daily rhythm can be opposed to a long, strong but obligatory one occurring in the presence of unsuitable substrate. Comparison between the two selection experiments showed that they led to similar phenotypes even for the non-selected trait. The correla- tion between traits could be due to pleiotropy of some major genes influencing the two traits. However, this phenomenon can be explained more simply by a common mechanism which becomes active in response to cues as different as unsuitable substrate or lighting. The selection may affect even the reactivity to environment or, more likely, the physiological mechanism controlling oviposi- 1150 Experientia 45 ( 1989). Birkhauser Verlag, CH-4010 Basel~S~itzcrland Research Articles tion. The genetic response to very unfavourable environ- ments <e\xeme stresses) has been investigated and most of the results can be explained by relatively few genes having brc'ad and mainly additive effects 16. 1 7 .  However, the egg retention affects the ovarian activity. and limits to selection would presumably be more severely canal- ized than those for specific actions of chemicals like ethanol o: insecticides. In our conditions, the poor sub- strate or :he photophase cannot be considered as stress- ful factor? since flies are normally submitted to photope- nod and are often deprived of oviposition sites as shown by their ox arian state in the field 18.  The capacity to stop oviposition must be a muscular, voluntan closing of the genital duct, under the control of the nenoiis system, since most of the females in our experiments presented one egg in the uterus. The genetic bases of i i s  egg-laying control need further investiga- lion. Ye\ ertheless, genetic variability between isofemale lines for both the oviposition rhythm and the response to an unsuiuble substrate has been demonstrated al- ready '- Ic'. Under natural conditions, the blocking capac- ity shows seasonal variations giving rise to an increasing frequenc? of flies with strong retention in the spring and in the autcrnn 14 .15 .  Such observations express the great genetic plasticity of this behaviour, which seems to be - selected by natural conditions (temperature.. .) in a few generations 14. The ability to control the oviposition process in response to various environmental factors, which can be as differ- ent as photoperiod or laying substrate, must allow Dro.sopI1ila females to adapt their response to environ- mental events, in particular by rapidly laying numerous eggs when conditions become more favourable. This trait might be particularly important for the population when the developmental sites are scarce and scattered, as is likely to be the case in temperate regions I s .  King, R. C..  Ovarian development in Droxophiln melunogu.sfer. Aca- demic Press. New York 1970. Grossfield. 1. in: The Genetic- and Biology of Drosophilu. vol. 2b, p. 1. Eds M. Ashburner and T. R. F. Wright. Academic Press. London 1978. David, J.. and Van Herreweae. 1. Bull. Biol. 150 (1971) 346. Richmond. R. C., and Gerkin.:. J. L., Behav. Genet. 9 (1979) 233. Takamura. T.. and Fuyama. V.. Behav. Genet. I0 (1980) 105. Chess, K. F.. and Ringo, J. M.. Evolution 39 (1985) 869. Allemand. R.. Biol. Behav. 8 11983) 231. Takamura. T., Jap. J. Genet. C (1980) 91. Boulktreau-Merle, J., and Temer. 0. .  Int. J. Inv. Rep. De\. 9 (1986) 113. Allemand. R., Fouillet. P.. and David, J. R., Genet. Sel. Evol. 16 (1984) 27. Bird, S. R.. and SemeonolT. R.. Genet. Res., Camb. 48 (1986) 151. Allemand. R.. J. Insect Physiol 22 (1976) 1031. Allemand. R., Biol. Behav. 8 I 1983) 273. Bouletreau-Merle, J;, Fouillet. P.. and Terrier, O., Ent. exp. appl. 43 (1987) 39. Boulktreau-Merle J., in: Advances in Invertebrate Reproduction, vol. 4, p. 461. Eds M. Porchei. J. C. Andries and A. Dhainaut. El- sevier, Amsterdam 1986. Parsons, P.. Aust. J. Zool. 3 11977) 693. Parsons, P. A., in: Evolutionary Biology, vol. 13, p. 175. Eds M. K. Hecht, W. C. Steere and B. Wallace. Plenum Publish. Corp. 1980. Boulktreau 1. Oecologia 35 (1978) 319. 

Correlated responses in lines of Drosophila melanogaster selected for different oviposition behaviours.

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Correlated responses in lines of Drosophila melanogaster selected for different oviposition behaviours.

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