John Jaenike

On optimal oviposition behavior in phytophagous insects.

Abstract A model is developed that predicts when an insect should oviposit on a potential larval host plant when it is encountered. Optimal behavior depends upon the suitability of this plant for larval development and on the probability of finding a more suitable host in the available time. This behavior is modeled for conditions in which the host either does or does not fluctuate in density.

Adaptation via Symbiosis: Recent Spread of a Drosophila Defensive Symbiont

Offsetting the Cost of Parasitism Fruit flies, like most animals, are vulnerable to infection by a range of organisms, which, in co-infections, can interact with sometimes surprising effects. Jaenike et al. (p. 212) discovered that a species of Spiroplasma bacterium that is sometimes found in flies, and that is transmitted from mother to offspring, protects its host from the effects of a nematode worm parasite, Howardula aoronymphium. The worm sterilizes the female flies and shortens their lives, but when flies were experimentally infected with Spiroplasma, their fertility was rescued. Similarly, in wild populations of fruit flies infected with worms, those also infected with Spiroplasma had more eggs in their ovaries. The bacterium inhibits the growth of the adult female worms, but such is the advantage of this bacterial infection in offsetting the burden of nematodes on reproductive fitness, Spiroplasma appears to be spreading rapidly through populations of fruit flies in North America. A bacterium protects fruit flies against a sterilizing worm parasite. Recent studies have shown that some plants and animals harbor microbial symbionts that protect them against natural enemies. Here we demonstrate that a maternally transmitted bacterium, Spiroplasma, protects Drosophila neotestacea against the sterilizing effects of a parasitic nematode, both in the laboratory and the field. This nematode parasitizes D. neotestacea at high frequencies in natural populations, and, until recently, almost all infections resulted in complete sterility. Several lines of evidence suggest that Spiroplasma is spreading in North American populations of D. neotestacea and that a major adaptive change to a symbiont-based mode of defense is under way. These findings demonstrate the profound and potentially rapid effects of defensive symbionts, which are increasingly recognized as major players in the ecology of species interactions.

Genetic Variation for Habitat Preference: Evidence and Explanations

Because adaptive shifts may often be initiated by evolutionary changes in behavior, it is of interest to determine the extent to which natural populations harbor genetic variation for ecologically important behaviors. Habitat preference is an especially significant behavior, because it determines the regime of natural selection acting on loci that affect adaptation to the environment. A survey of the literature reveals that genetic variation for habitat selection is common, especially in arthropods and mollusks, the groups that have been studied most frequently. Possible adaptive mechanisms by which this variation could be maintained within populations include a genetic correlation between density-independent fitness in a habitat and a preference for it; and soft selection, whereby density-dependent population regulation occurs independently in separate habitats. Several studies have documented a phenotypic correlation between preference and performance, but as yet, no such genetic correlations have been unequivocally demonstrated. We show theoretically that under hard selection, optimal habitat selection may often lower the probability of maintaining a polymorphism at a locus that affects adaptation to different habitats. Soft selection appears much more likely to promote variation for habitat preference. Mechanisms including resource competition and natural enemies whose numbers build up in a habitat-specific manner in response to host or prey density have the capacity to bring about selection favoring alleles whose carriers prefer relatively underused habitats. We believe that more progress in understanding the evolution of habitat preference will come from studies of these ecological mechanisms than from further demonstrations of the mere existence of genetic variation for such preferences.

Wolbachia and the evolution of reproductive isolation between Drosophila recens and Drosophila subquinaria

Endosymbiotic bacteria of the genus Wolbachia are widespread among insects and in many cases cause cytoplasmic incompatibility in crosses between infected males and uninfected females. Such findings have been used to argue that Wolbachia have played an important role in insect speciation. Theoretical models, however, indicate that Wolbachia alone are unlikely to lead to stable reproductive isolation between two formerly conspecific populations. Here we analyze the components of reproductive isolation between Drosophila recens, which is infected with Wolbachia, and its uninfected sister species Drosophila subquinaria. Laboratory pairings demonstrated that gene flow via matings between D. recens females and D. subquinaria males is hindered by behavioral isolation. Matings readily occurred in the reciprocal cross (D. quinaria females × D. recens males), but very few viable progeny were produced. The production of viable hybrids via this route was restored by antibiotic curing of D. recens of their Wolbachia symbionts, indicating that hybrid offspring production is greatly reduced by cytoplasmic incompatibility in the crosses involving infected D. recens males. Thus, behavioral isolation and Wolbachia‐induced cytoplasmic incompatibility act as complementary asymmetrical isolating mechanisms between these two species. In accordance with Haldanes rule, hybrid females were fertile, whereas hybrid males invariably were sterile. Levels of mtDNA variation in D. recens are much lower than in either D. subquinaria or D. falleni, neither of which is infected with Wolbachia. The low haplotype diversity in D. recens is likely due to an mtDNA sweep associated with the spread of Wolbachia. Nevertheless, the existence of several mtDNA haplotypes in this species indicates that Wolbachia have been present as a potential isolating mechanism for a substantial period of evolutionary time. Finally, we argue that although Wolbachia by themselves are unlikely to bring about speciation, they can increase the rate of speciation in insects.

Criteria for Ascertaining the Existence of Host Races

It may be asked why the process by which Phytophagic Species are formed is not reiterated on all hands, till Nature becomes a Babel of confusion and the number of distinct species equals the grains of sand on the sea-shore. The answer is simple. There are two great antagonistic forces in Nature, the Law of Variation, causing individuals of almost all species to assume occasionally abnormal characters or abnormal propensities, and what may be called the Law of Assimilation, which, by the intercrossing of these abnormal individuals and their descendants with the normal type, gradually in successive generations softens down, eliminates and extirpates whatever is strange and peculiar in them [Walsh (1864)].

ENVIRONMENTAL MODIFICATION OF OVIPOSITION BEHAVIOR IN DROSOPHILA

In order to assess the independent effects of larval and adult environments on oviposition site preference in four species of Drosophila (D. melanogaster, D. pseudoobscura, D. immigrans, and D. recens), individuals were exposed as larvae and/or adults to medium containing sodium chloride, ethanol, ethyl acetate, lactic acid, piperidine, or peppermint oil. For the first three species, previous exposure of adults to peppermint oil significantly reduced their aversion to this substance; that is, they appeared to become habituated to it. Adults of D. melanogaster also became habituated to 7% ethanol medium, which is normally repellent to ovipositing females. Finally, an induced preference for piperidine containing medium was exhibited by D. immigrans when they were exposed to such medium as adults. In no case did the larval environment have a significant effect on subsequent oviposition behavior. Buf if adults emerge in the vicinity of their larval environments, the processes of habituation and induced preference can promote local polyphagy, aid in the tracking of fluctuating resources, and facilitate the spread of genes that adapt individuals to particular larval food resources.

Competition in Natural Populations of Mycophagous Drosophila

In the northeastern United States, individual mushrooms commonly harbor the larvae of up to four species of Drosophila (D. falleni, D. recens, D. putrida, and D. testacea), as well as larvae of crane flies (Tipulidae), wood gnats (Anisopodidae), and other, small flies. An experiment showed that larvae of these species commonly exhaust the food in single mushrooms under natural conditions. Supplemental mushroom increased survival to adulthood in three Drosophila species and resulted in larger adult flies. There was substantial variation among individual mushrooms in the degree of food depletion by larvae; while some mushrooms were completely devoured, others appeared to provide more than enough food for the larvae. Mean body sizes of Drosophila that matured in nature were similar to those of flies reared in our experiments without supplemental food, which suggests that resource depletion and larval competition are common in natural populations of these species. (While the evidence for resource limitation is compelling, our methods do not allow us to distinguish between intraand interspecific competition.) As a result, fitness of flies in nature should vary greatly as a function of the amount of food available to larvae. We speculate that low rates of parasitism allow mycophagous Drosophila populations to deplete food resources more commonly than do phytophagous insects.

Host specificity, evolutionary relationships and macrogeographic differentiation among Ascaris populations from humans and pigs.

We describe a variety of restriction site polymorphisms in the introns of Ascaris nuclear genes and in the ribosomal DNA spacers. We use these markers, in addition to previously described mitochondrial variation, to clarify our understanding of the epidemiology of Ascaris in Guatemalan villages where humans and pigs occur in sympatry and to describe the genetic structure of host-associated Ascaris populations from world-wide locations. Intron sequences were amplified from individual worms and alleles defined by endonuclease digestion. Two loci were monomorphic, while 4 length variants and 22 point mutations were detected in the other 7 loci. Within sympatric Guatemalan populations no single locus from either the nuclear or mitochondrial genome was fixed for alternative alleles, although allele frequencies were significantly different at many loci. Phenograms constructed from multilocus nuclear genotypes of individual worms failed to reveal a single case of cross-infection, and demonstrate that divergent mtDNA genotypes are segregating within host-associated populations. On a world-wide scale, the data suggest that extant worm populations result from a single host shift, although characterization of genetic variation in additional loci will be necessary to confirm this. The direction and the geographical origin of the host shift were unresolved. Overall 65% of nuclear genetic variation was found within populations, host (human or pig) explained 18%, while geographical variation within host-associated populations explained 17%. The results (a) demonstrate the utility of introns for studying the epidemiology of parasites showing limited allozyme variation (b) suggest that programmes aiming to control Ascaris infection in the human population can safely ignore zoonotic infection from pigs and (c) illustrate the problems inherent in using single genetic markers to make inferences about the epidemiology of closely related parasite taxa.

Evolutionarily Stable Infection by a Male-Killing Endosymbiont in Drosophila innubila: Molecular Evidence From the Host and Parasite Genomes

Maternally inherited microbes that spread via male-killing are common pathogens of insects, yet very little is known about the evolutionary duration of these associations. The few examples to date indicate very recent, and thus potentially transient, infections. A male-killing strain of Wolbachia has recently been discovered in natural populations of Drosophila innubila. The population-level effects of this infection are significant: ∼35% of females are infected, infected females produce very strongly female-biased sex ratios, and the resulting population-level sex ratio is significantly female biased. Using data on infection prevalence and Wolbachia transmission rates, infected cytoplasmic lineages are estimated to experience a ∼5% selective advantage relative to uninfected lineages. The evolutionary history of this infection was explored by surveying patterns of polymorphism in both the host and parasite genomes, comparing the Wolbachia wsp gene and the host mtDNA COI gene to five host nuclear genes. Molecular data suggest that this male-killing infection is evolutionarily old, a conclusion supported with a simple model of parasite and mtDNA transmission dynamics. Despite a large effective population size of the host species and strong selection to evolve resistance, the D. innubila-Wolbachia association is likely at a stable equilibrium that is maintained by imperfect maternal transmission of the bacteria rather than partial resistance in the host species.

AGGREGATION AND THE COEXISTENCE OF MYCOPHAGOUS DROSOPHILA

SUMMARY (1) Intraspecific aggregation has been postulated to facilitate the coexistence of competing species that share patchy resources. Data on adult emergence numbers of four mycophagous species of Drosophila from field-collected mushrooms show that these species exhibit highly aggregated distributions, both in collections comprising several naturally occurring species of mushrooms and in those of a single species for which mushroom size, condition, exposure time, and location in the field were controlled. (2) The relation between the mean and the variance in the numbers of flies emerging per mushroom reveals that the mean level of larval crowding increases with overall population density. Aggregation of larvae of each species is due to (i) females laying eggs in clutches of more than one egg, and (ii) non-random distributions of ovipositing females across breeding sites. (3) The emergence number of different species of Drosophila tend to be positively correlated across mushrooms, especially between species belonging to the same species group. In fact, within species groups, intraspecific and interspecific aggregation of ovipositing females contribute about equally to the proportional increase in the number of competitors an individual larva shares a mushroom with. Thus, aggregation does not appear to play an important-role in the coexistence of species belonging to the same species group. (4) The probability of parasitism of emergent Drosophila by the nematode Howardula aoronymphium Welch is generally independent of emergence numbers. Thus, although density-dependent parasitism could promote coexistence of species that have independent aggregated distributions, we find little evidence of such density dependence in these species.