A. Symbiosis
A1. Defensive Symbiosis
A2. Obligate bacterial symbionts of parasitic nematodes
A3. Microbes of spotted wing drosophila
Intimate associations with microbes shape the lives of all multicellular organisms. Insects are no exception, and stand out for hosting an enormous diversity of symbiotic inherited bacteria that are transmitted from mothers to their offspring, often inside eggs. These bacterial endosymbionts play diverse and important roles in the ecology of their hosts, such as providing essential amino acids and vitamins, or protecting them against natural enemies. Others have evolved the ability to manipulate the reproduction of their hosts in order to increase the frequency of infected females (since only females transmit symbionts), for example by transforming males into females. Because most of these symbionts are cryptic and cannot be cultured outside of their hosts, they were little-studied before the recent revolution in gene sequencing.
A1. Defensive symbiosis
An exciting development in the study of infections is the realization that many organisms host symbiotic bacteria that help protect them against natural enemies. A major long-term goal of our lab is to understand the evolutionary and ecological consequences of these types of defensive symbioses. How pervasive and important are they in nature, compared to other modes of protection, such as insect immune systems or avoidance behaviours? Do hosts with defensive symbionts have weaker immune systems? And can natural enemies overcome defensive symbionts, and if so, how? We have focused on Spiroplasma bacteria that protect various species of Drosophila flies against parasitic nematodes and wasps. For example, without Spiroplasma symbionts, the woodland fly Drosophila neotestacea is sterilized by parasitic nematodes, whereas fertility is fully restored in flies with symbionts.
|
In fact, the benefit conferred by symbionts is so great (because nematode parasite infections are so common in nature), that symbiont-infected flies are replacing uninfected ones, and the infection is spreading rapidly across North America. We are interested in the ecological and evolutionary consequences of Spiroplasma spread on the entire community of organisms that interact with D. neotestacea. We also want to understand the mechanism of protection, and have recently discovered that Spiroplasma encodes diverse ribosome-inactivating protein toxins that appear to target parasite ribosomes. But we don’t yet understand how these toxins distinguish parasite cells and ribosomes from host ones; nor do we know how and whether some natural enemies are resistant to Spiroplasma.
Some recent papers:
-Ballinger MJ, Gawryluk RMR, Perlman SJ. 2019. Toxin and genome evolution in a Drosophila defensive symbiosis. Genome Biol. Evol. 11:253-262.
-Ballinger MJ, Perlman SJ. 2017. Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila. PLoS Pathogens, 13: e1006431.
-Hamilton PT, Peng F, Boulanger MJ, Perlman SJ. 2016. A ribosome-inactivating protein in a Drosophila defensive symbiont. Proc. Nat. Acad. Sci. USA. 113:350-355.
Some recent papers:
-Ballinger MJ, Gawryluk RMR, Perlman SJ. 2019. Toxin and genome evolution in a Drosophila defensive symbiosis. Genome Biol. Evol. 11:253-262.
-Ballinger MJ, Perlman SJ. 2017. Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila. PLoS Pathogens, 13: e1006431.
-Hamilton PT, Peng F, Boulanger MJ, Perlman SJ. 2016. A ribosome-inactivating protein in a Drosophila defensive symbiont. Proc. Nat. Acad. Sci. USA. 113:350-355.
A2. Obligate bacterial symbionts of parasitic nematodes
Many animals harbour obligate intracellular bacterial symbionts that have allowed them to adapt to entirely new niches, such as feeding on plant sap or animal blood, or to survive in hydrothermal vents in the deep sea. These obligate symbioses are often ancient and intimate, and neither partner can survive without the other. A major question is to understand how new obligate symbioses arise.
We recently discovered that Howardula aoronymphium, a common virulent nematode parasite of Drosophila flies, has recently acquired an obligate bacterial endosymbiont. This symbiont is in a group of bacteria called “Candidatus Symbiopectobacterium” that is closely related to a well-studied lineage of plant pathogens, called the Soft Rot Enterobacteriaceae, and that has repeatedly given rise to new symbioses in insects and nematodes. Our long-term goals are to determine the role of this new obligate symbiont. Does it provide its host with essential resources? Does it help its host overcome the fly’s immune system? How has a microbe that is so closely related to pathogens become an essential partner, and so quickly?
Some recent papers:
-Martinson VG, Gawryluk RMR, Gowen BE, Curtis CI, Jaenike J, Perlman SJ. 2020. Multiple origins of obligate nematode and insect symbionts by a clade of bacteria closely related to plant pathogens. Proc. Nat. Acad. Sci. USA. 117:31979-31986
-Martinson VG, Gawryluk RMR, Gowen BE, Curtis CI, Jaenike J, Perlman SJ. 2020. Multiple origins of obligate nematode and insect symbionts by a clade of bacteria closely related to plant pathogens. Proc. Nat. Acad. Sci. USA. 117:31979-31986
A3. Microbes of spotted wing drosophila
With Paul Abram (Research Scientist, Biological Control of Insect Pests, Agriculture & Agri-Food Canada), we are characterizing the infectious microbes of local Spotted Wing Drosophila (SWD), Drosophila suzukii, a major pest of berries and soft fruits. We are using next generation sequencing approaches to discover viruses of SWD. We are also examining the role of Wolbachia bacterial symbionts in SWD biology. Wolbachia bacteria are the most successful host-associated microbes on the planet, infecting ~40% of all insect species. Yet the strain of Wolbachia that infects SWD presents a mystery, because it is not known how or why the infection persists in nature. This project is funded by Genome British Columbia.
B. Selfish genetic elements
B1. Selfish X Chromosomes
B2. An unusual sex ratio distortion in a booklouse
Virtually all organisms harbour genomic parasites. These selfish genes violate the rules of Mendelian inheritance, often at the expense of their host, and have played a major role in shaping key host cellular and genetic processes. Yet they are largely understudied because their effects are often cryptic and/or they are suppressed by the rest of the genome. But the revolution in gene sequencing has greatly facilitated the discovery and characterization of new selfish elements. In addition, there is currently much interest in engineering selfish genetic elements to control pests and disease vectors; understanding the evolution and ecology of natural selfish genetic systems has great potential to help inform outcomes of these approaches.
B1. Selfish x chromosomes
Among the most striking selfish genetic elements are selfish sex chromosomes, and these have arisen independently many times in insects, rodents, and plants. Selfish X chromosomes have been reported in at least 20 different fly species. Male flies with a selfish X chromosome produce a gene product that kills or incapacitates sperm that carry a Y chromosome, and as a result, they produce almost only daughters. We are interested in the ecological, evolutionary and genetic consequences of selfish X chromosomes. How do they persist and what prevents their hosts from going extinct given the strong sex ratio distortion they produce? When and how does the host evolve to counteract distortion? We are also interested in understanding the genetic basis of selfish X chromosomes. We are addressing these questions using an ancient selfish X chromosome that we recently discovered in the woodland fly Drosophila testacea. This X chromosome is highly differentiated from standard X chromosomes, and we estimate that it diverged ~900,000 years ago. We have also recently found autosomal genes that suppress the action of the selfish X chromosome.
Some recent papers:
-Keais GL, Liu S, Perlman SJ. 2020. Autosomal suppression and fitness costs of an old driving X chromosome in Drosophila testacea. J. Evol. Biol. 33: 619-628.
-Keais GL, Hanson MA, Gowen BE, Perlman SJ. 2017. X chromosome drive in a widespread Palearctic woodland fly, Drosophila testacea. J. Evol. Biol. 30: 1185–1194.
Some recent papers:
-Keais GL, Liu S, Perlman SJ. 2020. Autosomal suppression and fitness costs of an old driving X chromosome in Drosophila testacea. J. Evol. Biol. 33: 619-628.
-Keais GL, Hanson MA, Gowen BE, Perlman SJ. 2017. X chromosome drive in a widespread Palearctic woodland fly, Drosophila testacea. J. Evol. Biol. 30: 1185–1194.
B2. An unusual sex ratio distortion in a booklouse
We have been studying an unusual selfish genetic element in an undescribed species of booklouse, Liposcelis sp. (booklice are the closest free-living relatives of parasitic lice and include many pests of stored grains) that we recently found in the Chiricahua Mountains in southern Arizona. Females that carry this selfish genetic element only ever produce daughters, and only ever transmit the chromosomes they inherited from their mothers. We are interested in understanding how females with the selfish genetic element coexist with their standard counterparts. We are also keen to determine the genetic basis of this unusual sex ratio and transmission distortion. |
Some recent papers:
-Hodson CN, Perlman SJ. 2019. Population biology of a selfish sex ratio distorting element in
a booklouse (Psocodea: Liposcelis). J. Evol. Biol. 32: 825-832.
-Hamilton PT, Hodson CN, Curtis CI, Perlman SJ. 2018. Genetics and genomics of an unusual selfish sex ratio distortion in an insect. Curr. Biol. 28: 3864–3870.
-Hodson CN, Hamilton PT, Dilworth D, Nelson CJ, Curtis CI, Perlman SJ. 2017. Paternal genome elimination in Liposcelis booklice (Insecta: Psocodea). Genetics. 206:1091-1100.
-Hodson CN, Perlman SJ. 2019. Population biology of a selfish sex ratio distorting element in
a booklouse (Psocodea: Liposcelis). J. Evol. Biol. 32: 825-832.
-Hamilton PT, Hodson CN, Curtis CI, Perlman SJ. 2018. Genetics and genomics of an unusual selfish sex ratio distortion in an insect. Curr. Biol. 28: 3864–3870.
-Hodson CN, Hamilton PT, Dilworth D, Nelson CJ, Curtis CI, Perlman SJ. 2017. Paternal genome elimination in Liposcelis booklice (Insecta: Psocodea). Genetics. 206:1091-1100.