Robert L. Unckless

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.

Population Extinction and the Genetics of Adaptation

Theories of adaptation typically ignore the effect of environmental change on population size. But some environmental challenges—challenges to which populations must adapt—may depress absolute fitness below 1, causing populations to decline. Under this scenario, adaptation is a race; beneficial alleles that adapt a population to the new environment must sweep to high frequency before the population becomes extinct. We derive simple, though approximate, solutions to the probability of successful adaptation (population survival) when adaptation involves new mutations, the standing genetic variation, or a mixture of the two. Our results show that adaptation to such environmental challenges can be difficult when relying on new mutations at one or a few loci, and populations will often decline to extinction.

Wolbachia as populations within individual insects: causes and consequences of density variation in natural populations

The population-level dynamics of maternally transmitted endosymbionts, including reproductive parasites, depends primarily on the fitness effects and transmission fidelity of these infections. Although experimental laboratory studies have shown that within-host endosymbiont density can affect both of these factors, the existence of such effects in natural populations has not yet been documented. Using quantitative PCR, we survey the density of male-killing Wolbachia in natural populations of Drosophila innubila females from the Chiricahua Mountains of Arizona. We find that there is substantial (20u2009000-fold) variation in Wolbachia density among wild flies and that within-host Wolbachia density is positively correlated with both the efficacy of male killing and maternal transmission fidelity. Mean Wolbachia density increases three- to five-fold from early to late in the season. This pattern suggests that Wolbachia density declines with fly age, a conclusion corroborated by a laboratory study of Wolbachia density as a function of age. Finally, we suggest three alternative hypotheses to account for the approximately lognormal distribution of Wolbachia density among wild flies.

Maintenance of a male-killing Wolbachia in Drosophila innubila by male-killing dependent and male-killing independent mechanisms.

Many maternally inherited endosymbionts manipulate their hosts reproduction in various ways to enhance their own fitness. One such mechanism is male killing (MK), in which sons of infected mothers are killed by the endosymbiont during development. Several hypotheses have been proposed to explain the advantages of MK, including resource reallocation from sons to daughters of infected females, avoidance of inbreeding by infected females, and, if transmission is not purely maternal, the facilitation of horizontal transmission to uninfected females. We tested these hypotheses in Drosophila innubila, a mycophagous species infected with MK Wolbachia. There was no evidence of horizontal transmission in the wild and no evidence Wolbachia reduced levels of inbreeding. Resource reallocation does appear to be operative, as Wolbachia‐infected females are slightly larger, on average, than uninfected females, although the selective advantage of larger size is insufficient to account for the frequency of infection in natural populations. Wolbachia‐infected females from the wild—although not those from the laboratory—were more fecund than uninfected females. Experimental studies revealed that Wolbachia can boost the fecundity of nutrient‐deprived flies and reduce the adverse effect of RNA virus infection. Thus, this MK endosymbiont can provide direct, MK‐independent fitness benefits to infected female hosts in addition to possible benefits mediated via MK.

Association between Wolbachia and Spiroplasma within Drosophila neotestacea: an emerging symbiotic mutualism?

Interspecific mutualism can evolve when specific lineages of different species tend to be associated with each other from one generation to the next. Different maternally transmitted endosymbionts occurring within the same cytoplasmic lineage fulfil this requirement. Drosophila neotestacea is infected with maternally transmitted Wolbachia and Spiroplasma, which are cotransmitted at high frequency in natural populations. Molecular phylogenetic evidence indicates that both endosymbionts have been present in D.u2003neotestacea for considerable evolutionary periods. Thus, conditions are suitable for the evolution of mutualism between them. In support of this possibility, there is a significant positive association between Wolbachia and Spiroplasma infection in many samples of D.u2003neotestacea from natural populations. Theoretically, such a positive association can result from either mutualism between these endosymbionts or recent spread. Collections from present‐day populations suggest that recent spread and mutualism have both operated to generate the positive association between Wolbachia and Spiroplasma. If selection acts on the combination of these two endosymbionts, they may be in the early stages of evolution of a more complex, cooperative association.

Population genetics of sexually antagonistic mitochondrial mutants under inbreeding.

In random mating populations, the fate of mitochondrial mutations with sexually antagonistic effects in males and females is based solely on their effects in females. Therefore, mitochondrial mutations that are beneficial for females but deleterious for males will be fixed in a deterministic model. Why then are males not less fertile? One among many several explanations is that inbreeding limits the ability of mutants to spread since the fitness of a mother is now linked to her sons fertility. We model this situation analytically and determine conditions under which such sexually antagonistic mitochondrial mutants can spread and fix in a population. We also provide alternative hypotheses for the lack of observed male sterility in natural populations.

The impact of nutrient loading from Canada Geese ( Branta canadensis ) on water quality, a mesocosm approach

A mesocosm experiment determined the impact of Canada Goose (Branta canadensis) feces on water chemistry. After 30 days of fecal additions (treatments of 1.209, 2.419 g, and 12.090 g every 3 d to 0.811 m3 size mescosms), no significant changes in water column total phosphorus, nitrate, N:P ratios, total Kjeldahl nitrogen, chlorophyll-a, or phycocyanin were observed among treatment groups. Soluble reactive phosphorus showed a marginally significant increase in the high treatment group. A settling experiment suggested that goose feces and associated nutrients settled quickly to the sediment. Since fecal material settles quickly to the sediment, the impact of additional fecal material would not become evident in a lake until a wind event mixes the sediment into the water column or through alteration of the productivity or community structure of the benthos.

A DNA Virus of Drosophila

Little is known about the viruses infecting most species. Even in groups as well-studied as Drosophila, only a handful of viruses have been well-characterized. A viral metagenomic approach was used to explore viral diversity in 83 wild-caught Drosophila innubila, a mushroom feeding member of the quinaria group. A single fly that was injected with, and died from, Drosophila C Virus (DCV) was added to the sample as a control. Two-thirds of reads in the infected sample had DCV as the best BLAST hit, suggesting that the protocol developed is highly sensitive. In addition to the DCV hits, several sequences had Oryctes rhinoceros Nudivirus, a double-stranded DNA virus, as a best BLAST hit. The virus associated with these sequences was termed Drosophila innubila Nudivirus (DiNV). PCR screens of natural populations showed that DiNV was both common and widespread taxonomically and geographically. Electron microscopy confirms the presence of virions in fly fecal material similar in structure to other described Nudiviruses. In 2 species, D. innubila and D. falleni, the virus is associated with a severe (∼80–90%) loss of fecundity and significantly decreased lifespan.

The Population Genetics of Adaptation: Multiple Substitutions on a Smooth Fitness Landscape

Much recent work in the theoretical study of adaptation has focused on the so-called strong selection–weak mutation (SSWM) limit, wherein adaptation is due to new mutations of definite selective advantage. This work, in turn, has focused on the first step (substitution) during adaptive evolution. Here we extend this theory to allow multiple steps during adaptation. We find analytic solutions to the probability that adaptation follows a certain path during evolution as well as the probability that adaptation arrives at a given genotype regardless of the path taken. We also consider the probability of parallel adaptation and the proportion of the total increase in fitness caused by the first substitution. Our key assumption is that there is no epistasis among beneficial mutations.

Isolation and characterization of 30 polymorphic microsatellite loci from the mycophagous fly Drosophila innubila

Drosophila innubila is a mushroom‐feeding member of the quinaria group, found in the woodlands and forests of the ‘sky islands’ in Arizona and New Mexico and extending south into central Mexico. Here, we describe and characterize 30 polymorphic microsatellite loci from D. innubila collected in the Chiricahua Mountains in Arizona. The number of alleles ranged from three to 21, and observed heterozygosity ranged from 0.0513 to 0.9737. Six loci were putatively X‐linked, six departed from Hardy–Weinberg equilibrium, seven had evidence of null alleles, and six showed evidence of linkage disequilibrium. These markers will be useful for examining population structure of D. innubila and its association with male‐killing Wolbachia.