Wolbachia pipientis , an agent of speciation?
"So, naturalists observe, a flea / Hath smaller fleas that on
him prey / And these have smaller fleas to bite 'em / And so
proceed ad infinitum.“
Jonathan Swift, of Gulliver's Travels
Made by Robin Groch
What is Wolbachia?
• Obligate endosymbiont bacteria
– a genus of the eubacteria domain
• Wolbachia is an α-proteobacteria
– descended from gram-negative bacteria
• Related to mitochondria
– also a gram-negative, fused to ancestor eukaryote 2 billion years ago
• Symbiont of Ecdyzoa (arthropods) and nematodes
• Cytoplasmically inherited rickettsiae that are found in reproductive
tissues (ovaries and testes)
Tree of Life
Alpha-Proteobacteria
Wolbachia
Wolbachia lost the
ability to cause
disease in
vertebrates
includes nitrogen-fixing bacteria,
chemoautotrophs, and
chemoheterotrophs. Members of this
sub-phylum grow at low-nutrient levels
(oligotrophic) and some have
stalks(prosthecae).
Distribution of Wolbachia
•
No vertebrates (humans included) are known to carry Wolbachia
•
infection is rampant in the invertebrate world (est. ~ 20 million species)
–
–
–
–
•
Estimates range from 15-20% of all insect species, 154 species so far
17 isopods and freshwater shrimp
Arachnids (mites and spiders)
Parasitic nematodes
Closest relative Wolbachia are a group of rickettsiae
– Ehrlichia equii, Ehrlichia canis, Cowdria ruminata, and Anaplasma marginale.
– These are blood parasites of mammals that are vectored by arthropods
•
Bacteria in the genus Rickettsia are still more distantly related
– genus includes several arthropod-vectored disease agents, including the
causative agents of Rocky Mountain spotted fever, murine typhus, and scrub
typhus, as well as a cytoplasmically inherited male-killing bacterium found in
ladybird beetles
Some of the Hosts of
Wolbachia
Achaera encedon
Drosophilia
Parasitic nematode
Nasonia
Armadillidium vulgare
Formica exsecta
Adalia bipunctata
Wolbachia Strains and their hosts
Nematodes
Arthropods
100 Mya
D*
C*
B (isopods and insects)
A (insects)
?? Mya
58-67 Mya
600 mya
100 Mya, proposed
time of endosymbiosis
of Wolbachia
*Strains C & D are found in filarial nematodes
Proposed horizontal transmission from arthropods to nematodes 100 mya
What is Wolbachia?
• Diversity of Behaviors
– Parasitism
• Manipulation of host reproduction in which one organism (the
parasite) lives in or on the body of another (the host) and obtains
nutrition and other benefit from it. A parasitic relationship is usually
to the detriment of the host but some host species have evolved
remarkable tolerance to high levels of parasitic infection
– Mutualism
• Wolbachia Hypothesized to help host metabolism, host benefits Wolbachia
has a home and a method of infectious transmission
– Commensalism
• loose association in which Wolbachia benefits with no apparent advantage
or disadvantage
Note: The boundaries between these three kinds of symbiosis are not
always clear because it can be difficult to establish advantage or
disadvantage in the relationship.
Filarial Worms: Mutualism Example
Filarial worms (nematodes are
associated with
Elephantiasis and Riverblindness diseases.
Wolbachia are parasites in
most invertebrates,
researchers suspect that they
live mutualistically with
nematodes. Perhaps the
clearest sign that the worms
derive some benefit from an
infection is the fact that they
suffer if their Wolbachia are
wiped out by antibiotics.
Onchocerca ochengi, a filarial
nematode in cattle, for
example, die when their
bacteria are destroyed. In other
species, the females simply
become sterile
Wolbachia and skewing the host’s
sex-ratio
Alteration of timing of host’s reproductive cycle results in a variety of
reproductive phenotypes :
•
Parthenogenesis (Infected virgins produce only daughters)
•
Male Killing (male embryos die, female embryos develop into infected
females)
– Hymenoptera
– Acraea encedon (Ugandan butterfly)
– Adelia bipunctata (two-spot ladybird)
•
Feminization (Infected genetic males reproduce as females)
•
Cytoplasmic Incompatibility (infected male and uninfected female yield no
viable embryos)
– Armadillidium vulagare (wood louse)
– Most common mechanism
Parthenogenesis Induction
•Infected virgins produce only daughters, score one for the symbiont
• Appears to be restricted to Hymenoptera (wasps)
• evidence of over 40 species affected
•Hymenoptera have particular sex determination “arrhenotoky” (males are
haploid, females diploid)
•Reversed with antibiotics
•Best case scenario for bacteria
•No superfluous males
•Mechanism
•Takes place in infected females unfertilized eggs
•1st mitotic division aborted in anaphase
•Yields 2N in unfertilized egg, therefore female
•Costs and Benefits for the host
•Infected females produce less offspring
•If bacteria completely successful, asexual reproduction results (bad for both)
•Older females harbor less Wolbachia (have laid more eggs)
•Older females produce more males.
Male Killing or “Dead Man Walking”
• Maternal inherited factors- kill male
progeny during embryogenesis
• High sex-ratio of females
• In Acraea encedon, 80-90 % population
female
• Wolbachia very adaptable
– Male killing in male heterogametic Adalia
– Male killing in female heterogametic Acraea
• Can reverse with antibiotics
Acraea encendana and leks
Sexist microbe. Wolbachia favor females, like this Ugandan butterfly,
because they will carry on the lineage. CREDITS: COURTESY OF BACCHI AND BANDI;
FRANCIS JIGGINS/CAMBRIDGE UNIVERSITY
Let’s Lek
• Sex-ratio shift towards females, bacteria
kills off males
• Now the males are choosy, a valuable
commodity
• Female role reversed, form dense swarms
(leks) (350 butterflies/200m²)
• Males prefer uninfected females, but
mistakes occur (which if fine with
Wolbachia)
Feminization
•
In Armadillidium individuals become
female unless androgenic gland
present
–
Gland produces androgenic hormones
to promote male sex determination
•
When Wolbachia is inherited from
female a suppression factor prevents
the formation of the gland
– converting males into
reproductively competent females
(although intersexes can also
produced).
•
•
•
Symbiont wins, all female offspring
Yum, Adalia eats unhatched males
Curable with antibiotics
Cytoplasmic Incompatibility
(CI)
• Wolbachia-induced CI is a reproductive incompatibility
between sperm and egg,
– which typically results in zygotic death in diploid species or male
production in haplodiploid species
– The bacteria are transmitted in eggs but are not transmitted
through sperm
• CI takes two forms, unidirectional and bidirectional.
– Unidirectional incompatibility typically occurs when the sperm
from a Wolbachia-infected male fertilizes an uninfected
– The reciprocal cross (uninfected male and infected female) is
compatible.
– Bidirectional incompatibility typically occurs when a male and a
female harbor different strains of Wolbachia that are mutually
incompatible egg.
CI Outcomes
Paternal Chromosome eliminated
embryo become haploid
Diploid organism
Haplodiploid organism
Embryo dies
CI mortality
If a wasp,
Normal male
Male-biased
Sex-ratio
Some mites, embryo
Dies, CI mortality
What’s Happening?
• Uninfected organisms
– Sperm enters egg
– Sperm chromatin
decondenses, forms
paternal pronucleus
– Paternal histones
removed and replaced by
female histones
– Replication commences,
chromosomes condense
for mitosis
– Paternal and maternal
pronuclei fuse to make
diploid nucleus of zygote
• Infected organisms
– Only female pronucleus forms
and undergoes first cleavage
– Paternal pronucleus does not
condense into individual
chromosomes
– Paternal chromosomes
appear as diffuse tangle of
chromatin and gets
fragmented during 1st mitotic
division
– If 2N organism, then embryo is
haploid, & either fails to
develop or female sterile or
has reduced fecundity
– Post-zygotic barrier
(aneuploidy or failure of
syngamy)
Modification-Rescue Model
of CI
•
•
Incompatibility apparently involves a two component system
bacterial "modification" of sperm and a bacterial "rescue" in the fertilized
egg.
– bacteria present in the testes modify the developing sperm (possibly via
chromatin binding proteins).
– The same bacterial strain must then be present in the egg to rescue this
modification. If rescue does not occur, then incompatibility between the egg and
sperm results.
– consistent with unidirectional incompatibility (modified sperm from infected males
are not rescued by uninfected eggs) and bidirectional incompatibility (different
bacterial strains use somewhat different modification-rescue systems).
•
Two general biochemical models have been proposed, either
– (a) Wolbachia in the male produce a product that disrupts sperm processing in
the egg (unless rescued) or
– (b) bacteria in the male act as a "sink" to bind away a product necessary for
normal processing of the sperm in the egg
– consistent with the "sink" hypothesis, a number of host chromatin-binding
proteins (such as H1 histone-like–protein) have been found to bind to Wolbachia
within host cells
Nasonia
Timing Is Everything for Wolbachia Hosts
Carl Zimmer (Science 296, 999-1000 (2002)
Cytoplasmic Incompatibility in
Nasonia “ A case of bad timing”
• Latest model:
– Asynchrony between maternal and paternal
pronuclei chromosomes during 1st mitosis
– Cause: CdK1/cyclin B and disruption of cell
cycle checkpoints
– Wolbachia inhibiting cell cycle timing in
unidirectional CI
• Infected sperm modified, no rescue in eggs
• Rescue = female pronucleus delayed also
“ A case of bad timing” continued
• Why do reciprocal matings work?
– Infected female have live Wolbachia which
can change the timing of the uninfected
sperm
• Why don’t bidirectional matings work?
– Males and females infected with different
strains that can’t align the timing of mitosis,
asynchrony still occurs…
Figure 1 Wolbachia and
cytoplasmic incompatibility.
Cytoplasmic incompatibility means
that when a male host infected
with Wolbachia (W+) mates with
an uninfected female (W- ), no
offspring are produced. All other
matings are fully compatible and
result in the production of
offspring. The consequence of this
system is that the maternally
transmitted Wolbachia tend to
spread through the host species.
Nature 409, 675 - 677 (2001) © Macmillan
Publishers Ltd. Evolution: Infectious speciation
MICHAEL J. WADE
A New Twist
•
Restoration of fertility in Sex-lethal
Drosophilia
•
infection with the parasite makes a
bad fly mutation more benign - but at
the cost of potentially addicting the
species to the parasite
•
Wolbachia probably produce
some protein that interacts with
the protein encoded by the sexlethal gene. The bacteria
apparently do not affect
expression of the gene or bypass
the protein in the pathway leading
to egg production
Wolbachia rescues oogenesis
defects
b, c, Ovaries from 4-day-old Wolbachia-infected
(b) or uninfected (c) Sxlf4/Sxlf4 females. Magnification 12
A host–parasite interaction rescues Drosophila oogenesis defects
DIANA J. STARR AND THOMAS W. CLINE . Nature 418, 76 - 79 (2002)
Infectious Speciation
• Wolbachia are known to alter early development
and mitotic processes in their hosts
• Wolbachia have implications for important
evolutionary processes. Of particular interest is
their potential role as a mechanism for rapid
speciation
• Wolbachia may promote rapid speciation by
causing reproductive incompatibility between
populations especially when bidirectional
incompatibility occurs.
Infectious Speciation (2)
• Post-zygotic barriers that are not germ-line
generated and reversible via antibiotics
• Quicker route to speciation
• Need earlier level of speciation… host
speciation
Figure 2 Genetic and infectious
models of speciation. a, A standard
genetic model in which the initial
state is an ancestral population of a
species that is homozygous at both
of two gene loci b, Infectious
speciation, which parallels the
genetic model. Reciprocal
cytoplasmic incompatibility between
WA males and WB females, and
WB males and WA females,
prevents hybridization, so in effect
the daughter populations are new
species even though they remain
genetically identical to one another
and to the ancestor.
Nature 409, 675 - 677 (2001) © Macmillan Publishers
Ltd. Evolution: Infectious speciation
MICHAEL J. WADE
Image Sources and Other
Miscellaneous Sources
•
Slide 1: Sexist microbe. Wolbachia favor females, like this Ugandan butterfly, because they will carry on the
lineage. CREDITS: COURTESY OF BACCHI AND BANDI; FRANCIS JIGGINS/CAMBRIDGE UNIVERSITY
•
•
Wolbachia (2) http://www.xrefer.com/entry.jsp?xrefid=645055 (Symbiosis definition)
Tree of Life: http://tolweb.org/tree?group=Eubacteria&contgroup=Life
•
Alpha-proteobacteria: http://www.life.umd.edu/classroom/bsci424/BSCI223WebSiteFiles/AlphaProteobacteria.htm
•
Filiaral worms: Zimmer, C. Wolbachia a tale of sex and survival. Science 292, 1093-1095 (2001).
•
Hosts in Wolbachia: Fruit fly www.mblab.gla.ac.uk/tubules/ gallery.html, Formica exsecta
www.cs.unc.edu/~hedlund/ FormicaDBout.html, Ugandan butterfly, CREDITS: COURTESY OF BACCHI AND
BANDI; FRANCIS JIGGINS/CAMBRIDGE UNIVERSITY, Filiaral worms: Zimmer, C. Wolbachia a tale of sex
and survival. Science 292, 1093-1095 (2001), www.nhm.ac.uk/.../photos/ armadillidium_vulgare.html, Adalia
bipunctata two-spot ladybug (ladybird) www.bio.umass.edu/biology/ alumni/biomass/vol03/
Wolbachia References
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Anderson, C.L., & Karr, T.L. Wolbachia: evolutionary novelty in a
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Wolbachia References
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Wolbachia References
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Ochman, H., & Moran, N.A. Genes lost and genes found: evolution of
pathogenesis and symbiosis. Science 292, 1096-1098 (2001).
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