John Jaenike - US grants

Drosophila have played a central role in the study of genetics, development, and evolution. Dr. Jaenike's research focuses on mushroom feeding species of Drosophila which are ideally suited to studies of the ecology and behavior of these insects. A primary concern of the proposed research will be with ecological interactions between these Drosophila and a species of nematode that parasitizes them. Because as many as 50% of these flies are parasitized at any time and because infected flies are seriously debilitated in terms of fertility, these nematodes have a substantial impact on populations of Drosophila. A series of field and laboratory studies will be used to investigate how nematodes affect survival, mating success, and competitive interactions of their Drosophila hosts. How ecological factors, such as ambient temperature, mushroom species, and Drosophila population densities, affect frequencies of parasites will also be examined. This research will provide basic information on the ecology of host-parasite interactions. In additions, because nematodes have the potential to be important agents for biological control of insects, this work could shed light on how best to carry out such control programs. Dr. Jaenike also has plans to study chromosomes which he has discovered to affect sex ratio in a species of Drosophila. Because "sex ratio" males sire only daughters, these chromosomes are expected in theory to increase in frequency and eventually cause population extinction. In reality, they do not do so. Dr. Jaenike will study ecological factors, including competitive ability and susceptibility to nematode parasitism, that may prevent the spread of these chromosomes. This research will provide insight on how selection at one level (chromosomes within individuals) is counteracted by selection at another level (individuals within populations).

Although parasites are ubiquitous and play an important role in most natural communities, they have generally been overlooked by population biologist. The almost complete lack of knowledge of the genetic structure of natural populations of parasites is particularly noteworthy. Genetic variation among parasites in their ability to infect various species of hosts is relevant to questions concerning (1) the effects of parasites on species diversity within communities, (2) the maintenance of genetic variation and sexual reproduction within host species, (3) host- parasite coevolution, and (4) modes of speciation in parasites. Such genetic variation may also be important in the evolution and ecology of zoonoses (parasites of animals that can infect humans) and pathogenic fungi that infect agricultural plants. The research proposed here focuses on a species of nematode, Howardula aoronymphium, that in nature parasitizes mushroom-feeding species of Drosophila. Previous studies have indicated that this nematode can have major effects on individuals, populations, and communities of flies. The proposed research includes: (1) a survey of natural populations of H. aoronymphium for genetic variation in infectivity, pathogenicity, and individual growth rate as a function of host species; and (2) selection experiments to determine how patterns of host availability affect the evolution of host specialization.

0074141
Jaenike


The proposed research will examine the evolution of associations between Drosophila and nematode parasites, encompassing time scales of evolutionary change from of millions of years down to changes ongoing within present-day populations. Experimental infections will be conducted with 8 nematode species and 24 Drosophila species. These experiments, in conjunction with molecular phylogenetic analyses, will allow a determination of the extent to which a parasite's host range is determined by host phylogeny, as well as determination of how host range evolves in these parasites. Closely related Drosophila species will be crossed to uncover the genetic basis of interspecific differences in resistance to parasites. These hybridization experiments will also reveal whether resistance to one parasite species is genetically correlated with resistance to others.

Parasites are ubiquitous - but generally overlooked - components of natural communities, often having major effects on the individuals and populations of their host species. The potential host range of a parasite is relevant to the issue of emerging diseases, the use of parasites in biological control programs, and the effect of invading parasites on endangered species. The proposed studies of the evolutionary determinants of parasite host range will contribute to the development of a comprehensive theory of host-parasite interactions.

Evolutionary ecology of male-killing Wolbachia in Drosophila innubila
Jaenike, John R.
University of Rochester

Wolbachia are intracellular, maternally transmitted, bacterial parasites present in the majority of insect species; their spread is accomplished by various means of manipulating host reproduction. Despite the potential ecological and evolutionary importance of Wolbachia, there has been very little research on Wolbachia dynamics and their effects on host insect populations in the field. This project focuses on the ecology of interactions between Drosophila innubila and the male-killing Wolbachia with which it is infected. Drosophila innubila inhabit mid- to high elevation forests in the sky islands of Arizona and New Mexico. Wolbachia cause almost 100% mortality of infected male embryos and infect a substantial fraction of females in these natural populations. This project will determine how the ecology of D. innubila allows the spread of male-killing Wolbachia. A series of field experiments will be carried out to assess whether infected flies suffer less competition than do uninfected flies. The project will also explore three mechanisms proposed to prevent fixation of male-killing Wolbachia within host populations: stochastic loss via incomplete maternal transmission, curing of the infection by antibiotic-containing mushrooms, and environmental temperature. Because D. innubila is distributed as isolated sky island populations, this species is ideal for investigating the effect of environmental gradients on Wolbachia dynamics. Finally, the project will quantify the effects of Wolbachia infections on the population-level sex ratio, mating frequencies, and sexual selection in D. innubila. It will specifically test predictions that the presence of male-killing Wolbachia at substantial infection frequencies results in a female-biased sex ratio in the population, lower rates of female mating, and selection on males to be discriminating in their choice of mates. The ecological focus of this proposal will contribute to understanding the dynamics of male-killing Wolbachia in natural populations and thus shed light on the feasibility of using these endosymbionts for deliberate manipulation of insect populations.

Wolbachia are maternally transmitted bacteria that are present in approximately 25% of all insects. Their spread is accomplished by various means of manipulating host reproduction, including asexual parthenogenesis and killing embryonic males. The spread of these infections is governed by the fidelity of maternal transmission and the effectiveness with which Wolbachia manipulates host reproduction. The proposed research will examine how environmental variables, including season, temperature, mushroom antibiotics, and fly age, affect the density of a male-killing Wolbachia within its host species, Drosophila innubila. The research will also quantify variation in Wolbachia density among flies in the wild and experimentally determine the relation between Wolbachia density and offspring sex ratio.

Wolbachia occur in some insects (such as mosquitoes and tsetse flies) that are vectors of important human diseases, and they related to bacteria (such as Rickettsia, Anaplasma, and Ehrlichia) that are pathogenic to humans and domesticated animals. The proposed research will contribute to understanding the dynamics of these infections in natural populations, about which very little is known. The novel component of this research is that it will connect the population dynamics of these infections at two levels: density variation within individual hosts and percent infection in populations of these hosts. The research may also lead to the discovery of new antibiotics.

Parasites are common throughout the natural world and most parasites spread by moving among individuals infectiously. Many insects, however, harbor microscopic parasites that are thought to be transmitted solely through the egg from mother to offspring. These microorganisms are termed reproductive parasites because they usually cause abnormalities during reproduction, such as feminization of males, killing of male embryos or development of embryos without fertilization. Most studies of reproductive parasites assume that transmission is strictly from mother to offspring. Surprisingly, recent experimental work has shown that these microorganisms can occasionally spread infectiously among unrelated individuals. The extent of infectious transmission in fruit flies (Drosophila) will be investigated by using DNA markers to detect transfer between individuals and between generations.

The research addresses fundamental process of disease and parasite transmission. Moreover, reproductive parasites such as those examined here have been proposed as biological control agents for some insect-vectored human diseases. If infectious transmission of the parasite is common, current models for pest control will need to be modified to prevent spread of the parasite to non-target insects. The investigators will continue to engage high school students and undergraduates in laboratory research and are developing outreach programs for high school and middle school students. This project is ideal for younger students because it is relatively simple conceptually, interesting (male-killing and feminization piques the interest of young students) and includes components that are technically simple.

Most species of insects are infected by symbiotic microorganisms, which spread either by directly benefiting their hosts or by manipulating host reproduction in ways that benefit the symbiont, but not the host. Bacterial Spiroplasma are among the more widespread of these symbionts. All Spiroplasma discovered to date either manipulate host reproduction or are pathogenic to their insect hosts. In populations of the fruit fly, Drosophila neotestacea, Spiroplasma have been found to confer resistance to nematode parasitism. Parasitized flies in the wild are essentially sterilized by the nematode if they do not carry Spiroplasma, but have nearly normal fertility if they are infected with these symbionts. This is the first finding of a beneficial effect of Spiroplasma on any insect species, and the first demonstration of an adverse effect of Spiroplasma on nematodes. Spiroplasma infection in D. neotestacea appears to have increased rapidly in the last 20 years in the eastern US and may be spreading westward. This project will conduct experiments to test for the effect of nematode parasitism on Spiroplasma infection dynamics within populations of D. neotestacea. Reciprocally, the effect of Spiroplasma on nematode parasitism in these flies will also be tested. Although most individuals of D. neotestacea in eastern North America are infected with Spiroplasma, none of the flies west of the Rockies are infected. This project will sample populations in British Columbia and Canadian Prairie Provinces, that were last sampled in 2002, to assess whether Spiroplasma is spreading westward across North America.

The fertility-restoring effect of Spiroplasma will also be tested on other combinations of Drosophila and nematode species. If general, such effects could be of great applied significance. River Blindness and Elephantiasis are caused by filarial nematodes that are transmitted by blackflies and mosquitoes. If Spiroplasma confers resistance to filarial nematodes, then Spiroplasma could spread within populations of the insect vectors, which might reduce nematode reproduction and thus incidence and severity of filarial diseases. In principle, a relatively simple manipulation of the insect vectors could yield great public health benefits. This project will provide research training for undergraduate and graduate students.

Most insect species on earth carry specific bacteria that are passed from infected females to their offspring. Many of these bacteria are beneficial to their hosts in such ways as conferring resistance to pathogens. Because insects are important members of larger ecological communities, the bacteria they carry may affect the structure and dynamics of these communities. The proposed research will examine several community-level effects of specific bacteria that infect specific mushroom-feeding flies. The bacteria living inside flies confer resistance to the sterilizing effects of a parasitic nematode worm and thus increase the fitness of parasitized flies. In addition, the bacteria dramatically affect the population dynamics of these parasitic nematodes: nematode parasitism increases rapidly in fly populations that lack bacteria, but the nematodes quickly go extinct in bacteria-infected populations. This project will investigate three questions: 1) How do bacteria affect the relative abundance of various species of competing flies, both in the presence and absence of nematode parasitism? 2) How does the presence of bacteria in one fly species affect the rate of nematode parasitism in other fly species? 3) Under what conditions can bacteria spread to new fly species?

This research has potential broader impacts in the areas of public health and agriculture. Filarial nematodes cause onchocerciasis (River Blindness) and lymphatic filariasis in humans, with about 160 million people currently infected worldwide. These nematodes are carried from one person to another by insect vectors. If specific bacteria adversely affect nematodes within insect vectors, it might be possible to introduce the bacteria into populations of these insects and thus reduce the transmission, prevalence, and severity of certain diseases. As a potential agricultural application, bacteria or genes derived from them could be introduced to crop plants to provide resistance to root-knot nematodes, which annually cause over $120 billion in agricultural damage around the world. The proposed work includes several projects suited to undergraduate research. The PI will work with the Kearns Center at the University of Rochester to recruit low-income, first-generation, and underrepresented minority students.

The cooperative relations between animals and their symbiotic bacteria make a crucial contribution to global diversity, but there remains a major gap in our understanding of how the taxonomic diversity (number of species etc.) relates to its functional diversity (what organisms do). In this project, genetic measures of diversity will be applied to quantify the taxonomic and functional diversity of bacterial communities in fruit flies and their relatives. A century's worth of genetic research on fruit flies makes these species a particularly amenable study system. This project will use several fly species, including an emerging agricultural pest that feeds on fruit and mushrooms, to investigate how taxonomy and function of the bacteria are coupled both to each other and to the functional diversity of the flies. The impact of these interactions on the capacity of the flies to utilize and damage fruits, their competitive interactions, and their resistance to parasites, will also be investigated. The research will also use genomic methods to obtain an integrated understanding of how animal-bacterial interactions shape the taxonomic and functional diversity of both the animal and its microbiota.

This project will provide research education in biodiversity science for two postdoctoral associates and graduate and undergraduate students, and will be communicated to the general public by Science Saturday meetings, including talks and hands-on demonstrations, at the Rochester Museum and Science Center. A photographic exhibition communicating the beauty, complexity and diversity of animal-microbial associations will be organized at Cornell University for the general public. Both these complementary initiatives have plans for traveling exhibitions, for wider dissemination of the importance of biodiversity. The insects studied in this project include an invasive pest, the spotted-wing drosophila. The researchers will enhance ongoing extension activity via meetings, newsletter articles, and interviews with local media to describe how the findings of this research may help to mitigate the damage of this insect to crop production and food quality.