Roland Allemand

Ecological and genetic interactions in Drosophila-parasitoids communities: a case study with D. melanogaster, D. simulans and their common Leptopilina parasitoids in south-eastern France

Drosophila species are attacked by a number of parasitoid wasps, which constitute an important factor of population regulation. Since Drosophila melanogaster and Drosophila simulans share common parasitoid species, their ecology and evolution can hardly be understood without considering parasitoids. After a short review of data available on Drosophila–parasitoid interactions involving D. melanogaster and D. simulans as hosts, we report field and laboratory experiments investigating the ecological role of Leptopilina parasitoids in Drosophila communities of southern France. Seasonal survey of species abundance shows that strong interspecific interactions occur at both tropic levels. D. simulans progressively replaces D. melanogaster in southern areas suggesting competitive displacement. Parasitoids are responsible for very high Drosophila mortality (up to 90% in some fruits). Field data emphasize the importance of selective pressure that parasitoids exert on Drosophila communities. The two Leptopilina parasites (L. heterotoma and L. boulardi) have different local abundances, which vary in time, and they also compete for hosts. We show that parasitoids can mediate the coexistence of D. melanogaster and D. simulans in the laboratory, and thus may contribute to their puzzling coexistence in the field. Conversely, hosts exert selective pressures on parasitoids, and development on either D. melanogaster or D. simulans strongly affects fitness of adult wasps in a temperature-dependent fashion. Local variation in host species abundance and diversity could thus account for the genetic differentiation we observed in one parasitoid species. Despite laboratory studies cannot fully explain complex field situations, it is clear that the ecology and evolution of Drosophila populations and communities, especially D. melanogaster and D. simulans, are strongly constrained by parasitoids, which should receive more attention.

Ecology and life history evolution of frugivorous Drosophila parasitoids.

Parasitoids and their hosts are linked by intimate and harmful interactions that make them well suited to analyze fundamental ecological and evolutionary processes with regard to life histories evolution of parasitic association. Drosophila aspects of what parasitoid Hymenoptera have become model organisms to study aspects that cannot be investigated with other associations. These include the genetic bases of fitness traits variations, physiology and genetics of resistance/virulence, and coevolutionary dynamics leading to local adaptation. Recent research on evolutionary ecology of Drosophila parasitoids were performed mainly on species that thrive in fermenting fruits (genera Leptopilina and Asobara). Here, we review information and add original data regarding community ecology of these parasitoids, including species distribution, pattern of abundance and diversity, host range and the nature and intensity of species interactions. Biology and the evolution of life histories in response to habitat heterogeneity and possible local adaptations leading to specialization of these wasps are reported with special emphasis on species living in southern Europe. We expose the diversity and intensity of selective constraints acting on parasitoid life history traits, which vary geographically and highlight the importance of considering both biotic and abiotic factors with their interactions to understand ecological and evolutionary dynamics of host-parasitoid associations.

Adaptive significance of a circadian clock: temporal segregation of activities reduces intrinsic competitive inferiority in Drosophila parasitoids.

Most organisms show self–sustained circadian oscillations or biological clocks which control their daily fluctuations in behavioural and physiological activities. While extensive progress has been made in understanding the molecular mechanisms of biological clocks, there have been few clear demonstrations of the fitness value of endogenous rhythms. This study investigated the adaptive significance of circadian rhythms in a Drosophila parasitoid community. The activity rhythms of three sympatric Drosophila parasitoids are out of phase, the competitively inferior parasitoid species being active earlier than the superior competitor. This temporal segregation appears at least partially determined by endogenous periods of the clock which also vary between species and which correlate the time of activity. This earlier activity of the inferior competitor significantly reduces its intrinsic competitive disadvantage when multiparasitism occurs, thus suggesting that natural selection acting on the phase of the rhythm could substantially deviate the endogenous period from the optimal ca. 24 h period. This study demonstrates that temporal segregation of competing species could be endogenously controlled, which undoubtedly favours their coexistence in nature and also shows how natural selection can act on biological clocks to shape daily activity patterns.

Comparative life histories and ecophysiology of Drosophila melanogaster and D. simulans

Numerous laboratory investigations have compared Drosophila melanogaster and D. simulans for various life history traits and fitness related ecophysiological parameters. From presently available information, it is however difficult to get a general comparative pattern describing the divergence of their ecological niches and understanding their demographic success. Two environmental factors seem however to have played a major role: temperature and alcoholic resources. From an ecophysiological approach, D. simulans may be described as generally more sensitive to stresses; other results point to this species as more cold adapted than its sibling; in some cases, however, D. simulans may appear as better adapted to a warm environment. When investigated, ecophysiological traits show a lesser geographic variability in D. simulans than in D. melanogaster. Presently available information does not explain the ecological prevalence of D. simulans in many places with a mild temperate or subtropical climate. This is presumably due to the fact that most comparisons have been done at a single, standard temperature of 25°C. Comparative studies should be undertaken, spanning the thermal ranges of the two species, and the phenotypic plasticity of ecophysiological traits should now be considered.

Les rythmes de vitellogenese et d'ovulation en photoperiode LD 12:12 de Drosophila melanogaster

Resume Under photoperiodic conditions (LD 12:12), a rhythm of oviposition was observed with an important peak at the beginning of the scotophase. The ovarian state of females submitted to such conditions was analysed by dissections every two hours during two successive days. A cyclic variation (with a period of 24 hr) was observed in the frequencies of egg chambers in early vitellogenesis. end of vitellogenesis and of mature oocytes. Every day, numerous egg chambers begin their vitellogenesis in the second half of the photophase. Then, the maximum frequencies of the successive stages of vitellogenesis are observed successively with time. At the end of the next photophase, numerous mature oocytes are retained within the ovaries so that an important oviposition is possible at the beginning of the darkness. These results allow an estimation of the duration of vitellogenesis (about 12.5 hr at 25°C) and of oocytes retention (maximum duration 6 hr).

Behavioural circadian rhythms measured in real-time by automatic image analysis: applications in parasitoid insects

Abstract. A video analysis system was developed to study behavioural circadian rhythms in insects. Technical innovations were performed in image analysis and in the use of robotics. In image analysis, both the automatic detection of the insect and the calculation of several variables (linear and angular speed, locomotor activity, etc.) are carried out in real‐time, which saves time and allows long‐term studies without any intervention of the operator. The displacement of the camera by robotics allows the simultaneous study of many individuals (i.e. sixty individuals for the study of locomotor activity of adult insects, more than 400 individuals for the study of the emergence of adult parasitoids from their host). Four applications of this new device are presented. They deal with circadian rhythms in parasitoid insects: locomotor activity and time variation in locomotory parameters, daily distribution of the emergence and onset of the locomotor activity in adults. The adaptability of the system to several experimental materials and situations is discussed and the interest of the study of behavioural rhythms in the approach of host‐parasitoid associations is emphasized.

Variability of venom components in immune suppressive parasitoid wasps: From a phylogenetic to a population approach

Endoparasitoid wasps develop at the expense of other insects, leading to their death. Eggs deposited inside the host body induce an immune response, which results in the formation of a melanized cellular capsule around the egg. To evade or counteract this response, endoparasitoids have evolved different strategies, the most often reported being injection into the host of immunosuppressive factors, notably venom proteins, along with the egg. The analysis of venom components has been performed independently in species of different taxa, but the present picture is far from complete. Intriguingly, the question of the level of venom variability inside species has been neglected, although it may partly determine the potential for parasitoid adaptation. Here, we present a short review of our present knowledge of venom components in endoparasitoids, as well as of the only well-known example of intraspecific variability in a venom immune suppressive protein being responsible for variation in parasitoid virulence. We then present data evidencing inter-individual variation of venom protein profiles, using a gel electrophoresis approach, both in laboratory strains and field populations of a figitid and a braconid species. Whether occurrence of such variability may permit a selection of parasitoid venom components driven by the host remains to be tested, notably in the context of the production and use of biological control auxiliaries.

Influence de modifications des conditions lumineuses sur les rythmes circadiens de vitellogenese et d'ovulation chez Drosophila melanogaster

Abstract Under photoperiodic conditions (LD 12:12), a rhythm was observed in the frequencies of ovarian egg chambers and of mature oocytes. Females reared and kept in permanent darkness (DD) did not show any rhythm. After a transition from LD 12:12 to DD, the rhythm of vitellogenesis remained almost unchanged for at least 5 days while the rhythm of oocytes retention disappeared. Suppression of a suitable oviposition substrate resulted in an accumulation of mature oocytes in the ovaries. When a conveneint medium was given again, the egg-laying proved to be highly dependent on the light conditions. Most of the oocytes remained in retention during the light phase. Significant egg-laying only occurred after the beginning of darkness. In such conditions females can lay one egg every 3 min. The egg-laying rhythm observed under cyclic light conditions thus arises from two separate physiological processes: oocyte production (vitellogenesis) which has a circadian, endogenous rhythm and oviposition which is directly dependent on the light conditions.

Prevalence of a virus inducing behavioural manipulation near species range border

The densities of conspecific individuals may vary through space, especially at the edge of species range. This variation in density is predicted to influence the diffusion of species‐specific horizontally transmitted symbionts. However, to date there is very little data on how parasite prevalence varies around the border of a host species. Using a molecular epidemiology approach, we studied the prevalence of a vertically and horizontally transmitted virus at the edge of the geographic range of its insect host, the Drosophila parasitoid wasp Leptopilina boulardi. L. boulardi is a Mediterranean parasitoid species showing a recent range expansion to the north (in France). The LbFV virus manipulates the behaviour of females, increasing their tendency to lay additional eggs in already parasitized Drosophila larvae (superparasitism). This is beneficial for the virus because it allows the virus to be horizontally transferred during superparasitism. We show that LbFV prevalence is very high in central populations, intermediate in marginal populations and almost absent from newly established peripheral populations of L. boulardi. We failed to detect any influence of temperature and diapause on viral transmission efficiency but we observed a clear relationship between prevalence and parasitoid density, and between parasitoid density and the occurrence of superparasitism, as predicted by our epidemiological model. Viral strains were all efficient at inducing the behavioural manipulation and viral gene sequencing revealed very low sequence variation. We conclude that the prevalence reached by the virus critically depends on density‐dependent factors, i.e. superparasitism, underlying the selective pressures acting on the virus to manipulate the behaviour of the parasitoid.

Genetic analysis of the circadian oviposition rhythm inDrosophila melanogaster: Effects of drift in laboratory strains

Under photoperiodic conditions, flies recently collected in nature exhibit, at the beginning of the scotophase, an oviposition peak which has a higher amplitude in Afrotropical than in European temperate populations. Several old laboratory strains failed, however, to show this peak. In each cross between genetically different strains, the oviposition curves of F1 and F2 were usually close to the midparent curve. Ten isofemale lines from an Afrotropical populations were submitted to inbreeding and drift. After 100 generations, two of the four surviving lines had retained the high peak typical of the origin population while the two others had lost it. Chromosome substitutions between these lines demonstrated a polygenic inheritance with a significant effect of the three major chromosomes. Presumably, the variations of amplitude of the oviposition peak were not caused by a modification of the ovarian activity but by a behavioral change toward the external signals of the environment.