Evolution of Obligate Specialist Species: How Changes to a Single Gene Restricted Drosophila pachea to a Single Species of Cactus

Contributed by: Steve Schaeffer

             The hormone ecdysone regulates many developmental processes during metamorphosis in insects.  In most Drosophila species, cholesterol is the initial substrate for the pathway that synthesizes ecdysone.  A recent study by Lang et al. (2012) provides evidence that amino acid substitutions in the neverland gene are responsible for an adaptive host shift of a Drosophila species. The enzyme produced by the neverland gene converts cholesterol to 7-dehydrocholesterol in the initial step in the ecdysone pathway.  Drosophila pachea lives exclusively on senita cactus (Lophocereus schottii).  The senita cactus lacks appreciable levels of cholesterol, but does have other sterols such as lathosterol that could be used to make ecdysone.  The neverland enzyme of Drosophila pachea is unable to make 7-dehydrocholesterol from cholesterol, which results from two to four amino acid changes in residues that are strongly conserved among Drosophila species. Lang et al. (2012) used transgenic experiments in Drosophila melanogaster neverland knockdown mutants to test the activity of the D. pachea neverland extant and inferred proteins with a variety of sterols.  The ancestral neverland proteins were able to convert both cholesterol and lathosterol into 7-dehydrocholesterol while only lathosterol is used by the extant D. pachea enzyme to make 7-dehydrocholesterol.  A population genetics analysis shows that nucleotide diversity in the neverland gene region is consistent with a recent selective sweep.  This study is a nice example of an integrative study that used molecular and population genetic analysis to show how changes to a single enzyme can result in a species being an obligate specialist.  In this case, D. pachea became an obligate specialist on senita cactus.  This change may have allowed D. pachea to have fewer competitors on its new host.  While this change may currently be advantageous, if availability of the host is reduced, D. pachea could be an evolutionary deadend.

Abstract Most living species exploit a limited range of resources. However, little is known about how tight associations build up during evolution between such specialist species and the hosts they use. We examined the dependence of Drosophila pachea on its single host, the senita cactus. Several amino acid changes in the Neverland oxygenase rendered D. pachea unable to transform cholesterol into 7-dehydrocholesterol (the first reaction in the steroid hormone biosynthetic pathway in insects) and thus made D. pachea dependent on the uncommon sterols of its host plant. The neverland mutations increase survival on the cactus’s unusual sterols and are in a genomic region that faced recent positive selection. This study illustrates how relatively few genetic changes in a single gene may restrict the ecological niche of a species.

Reference

Lang, M., S. Murat, A. G. Clark, G. Gouppil, C. Blais, L. M. Matzkin, É. Guittard, T. Yoshiyama-Yanagawa, H. Kataoka, R. Niwa, R Lafont, C. Dauphin-Villemant, and V. Orgogozo. 2012 Mutations in the neverland gene turned Drosophila pachea into an obligate specialist species. Science 337: 1658-1661.

Probing the Origin of Multicellularity in a Test Tube

Contributed by: Jianzhi Zhang

The evolution of multicellularity is undoubtedly one of the most important events in the history of the Earth. Although multicellularity originated multiple times, all occurred long ago and no transitional form exists today. Thus, there is little information about the key steps that led to these transformative evolutionary events. While the origin of multicellularity may sound very complex, a recent study showed that primitive forms of multicellularity can emerge from unicellularity within a matter of weeks in test tubes, when the “environment” is right.

Ratcliff et al. (1) used gravity to select yeast cells that stick together and thus settle more quickly than separated cells. After just 60 rounds of selection, the yeast population is dominated by snowflake-like phenotypes, with a new life history characterized by reproduction via multicellular propagules, a juvenile phase, and determinate growth. However, the genetic changes responsible for the new phenotype are unknown. Given the ease of sequencing yeast genomes, it would be of great interest to identify the causal mutations, which will allow a molecular understanding of such primitive multicellularity.

            In an earlier study that is somewhat less dramatic but more elegant, Koschwanez et al. (2) studied the condition under which multicellularity is favored over unicellularity, by creating an environment in which cells need to cooperate to be able to survive and reproduce. To use sucrose as the sole carbon source, yeast expresses an enzyme called invertase in the cell wall to degrade sucrose into glucose and fructose. These monosaccharides unfortunately diffuse into the environment and need to be re-absorbed by yeast cells. One can imagine that under a low sucrose concentration, a single cell in a test tube would not be able to survive because most of the monosaccharides produced are diffused and wasted. When the cell density increases, the monosaccharide concentration in the environment rises, which may be able to support yeast growth. This was indeed demonstrated experimentally. Furthermore, the authors found mutant yeasts whose cells fail to separate after mitosis to be fitter than the wild-type yeast under certain parameters of cell density and sucrose concentration. Thus, a single mutation may initiate the path to multicellularity.   

Molecular dissections of microevolutionary changes are becoming routine, thanks to rapid progress in molecular genetics and genomics. But big, transformative changes seen in macroevolution remain largely unexplained in terms of their molecular genetic basis. The very micro evolutionary experiments in test tubes may prove instrumental in unlocking the mysteries of macroevolution.

References

1. Ratcliff WC, Denison RF, Borrello M, Travisano M. 2012. Experimental evolution of multicellularity. Proc Natl Acad Sci U S A. 109:1595-600.

2. Koschwanez JH, Foster KR, Murray AW. 2011. Sucrose utilization in budding yeast as a model for the origin of undifferentiated multicellularity. PLoS Biol. 9:e1001122.

Drosophila Self-medicates Itself against Parasitoid Wasps

Contributed by: Steve Schaeffer

           Hosts use a variety of strategies to deal with a never ending battle with its parasites.  Larvae of Drosophila species are often infected by parasitoid wasps and feeding by the wasp larvae lead to the eventual death of fly larvae.  A recent study by Milan et al. (2012) published in Current Biology shows that fly larvae take advantage of environmental alcohols to limit the infection of parasitoid wasp larvae.  The work shows that consumed alcohol leads to the death of the wasp larvae.  In addition, Drosophila larvae seek out alcohol when infected by the parasite in an effort to self-medicate itself against the invader.  How this story develops will be interesting in light of the well-known polymorphism in the alcohol dehydrogenase gene in Drosophila melanogaster.  It will be interesting to know if the different alleles of Adh change the effectiveness of the self-medication or the behavior.

Abstract Plants and fungi often produce toxic secondary metabolites that limit their consumption [1-4], but herbivores and fungivores that evolve resistance gain access to these resources and can also gain protection against nonresistant predators and parasites [3, 5-8]. Given that Drosophila melanogaster fruit fly larvae consume yeasts growing on rotting fruit and have evolved resistance to fermentation products [9, 10], we decided to test whether alcohol protects flies from one of their common natural parasites, endoparasitoid wasps [11-13]. Here, we show that exposure to ethanol reduces wasp oviposition into fruit fly larvae. Furthermore, if infected, ethanol consumption by fruit fly larvae causes increased death of wasp larvae growing in the hemocoel and increased fly survival without need of the stereotypical antiwasp immune response. This multifaceted protection afforded to fly larvae by ethanol is significantly more effective against a generalist wasp than a wasp that specializes on D. melanogaster. Finally, fly larvae seek out ethanol-containing food when infected, indicating that they use alcohol as an antiwasp medicine. Although the high resistance of D. melanogaster may make it uniquely suited to exploit curative properties of alcohol, it is possible that alcohol consumption may have similar protective effects in other organisms.

References

1. Milan, N.F., Kacsoh, B.Z., Schlenke, T.A. 2012. Alcohol Consumption as Self-Medication against Blood-Borne Parasites in the Fruit Fly. Current Biology 22(6):488-493.