1. Increasing our
knowledge of schistosome diversity
In
the phylum Platyhelminthes, class Trematoda, subclass Digenea, there are ~2,500
genera, and ~18,000 species of digenetic trematodes worldwide. This represents
one of the largest groups of internal metazoan parasites, second only to the
nematodes. Digenetic trematodes are obligate adult parasites in most vertebrate
definitive hosts, several phyla as second intermediate hosts, and mollusks as
first intermediate hosts. As a result these parasites inhabit a staggering
number of phyla and classes of animals, sometimes even plants, and
have occupied
nearly every organ in its host. This fact has attracted the attention of
researchers across a broad range of disciplines, especially since many of these
schistosomes are etiological agents of human and domesticated animal
diseases. One
of the most distinctive superfamilies of trematodes is the
Schistosomatoidea, which
includes the Schistosomatidae in birds and mammals, Spirorchiidae in turtles,
Sanguinicolidae in fishes and Clinostomidae in birds. Members of the
Schistosomatidae
are unique digeneans that are morphologically distinct with a number of
features that set them apart from the rest of the subclass. Most notable, they
are dioecious, dimorphic and have a 2-host life cycle: bird or mammal
and snail. Schistosomes are primarily associated with freshwater
habitats and are
found in all temperate and tropical regions of the world. The
monophyly of the family
is well-supported and includes about 90 species in 15 genera and 4 subfamilies.
Schistosomes are of
particular concern as they cause
morbidity and mortality in humans that has placed them as a study
priority, much of which is focused
on genomics,
control and drug resistance, but not taxonomy! Human
schistosomiasis remains
one of the world's great-unconquered, infectious helminth diseases. Morbidity
and mortality rates have remained high (200 million infected, 130,000
deaths/year). Another schistosome zoonosis, cercarial dermatitis,
known as "swimmer's
itch", is an ailment caused by the penetration of human skin by the cercariae
of non-human schistosome parasites is a common, recurrent phenomenon in aquatic
habitats worldwide.
Most cases of dermatitis originate from schistosome species of waterfowl. Other
than the medically important mammalian genus Schistosoma, much remains to be learned about
global species diversity, biogeography, patterns of vertebrate and snail host
usage, and evolutionary relationships of the other schistosome genera. We need
a precise determination of species that is valuable not only from a biological
view, but also as a tool to predict health risks.
The
aim of this project is an ongoing effort to incorporate new sequence and/or
morphological data from schistosome samples into the existing phylogeny of the
blood flukes. There are many areas in the world where the diversity of
schistosome worms, from either snails or vertebrates, has been insufficiently
sampled. Further illumination of schistosome biology will also be provided by
more complete sampling of other blood fluke families, the Spirorchiidae from
turtles generally considered the sister family of Schistosomatidae, and the
Sanguinicolidae, the blood flukes of fishes. Thus far, we have collected
samples from Sri Lanka (R.P.V.Jayanthe
Rajapakse,
Dept. Veterinary Pathology), Australia and Kenya (Dr. Gerald Mkoji).
Figure from Brant SV, Loker ES. 2005. Can specialized
pathogens colonize distantly related hosts? Schistosome evolution as a case
study. PLoS Pathogens 1(3): e38.
2.
Systematics of avian schistosomes with a focus on
Trichobilharzia
Why avian schistosomes? Avian schistosomes comprise the
largest and most diverse clade in the family (Brant et al. 2006). These schistosomes are
ecologically restricted to waterbirds as definitive hosts, and most use
freshwater snails as intermediate hosts. Avian schistosome species commonly
cause cercarial dermatitis in all parts of the world except Antarctica. In
addition to their medical impact, these outbreaks can have significant economic
repercussions (e.g. tourism, real estate) for affected communities. Avian schistosomes that
are responsible for dermatitis outbreaks are poorly characterized; even in the
U.S. we lack reliable information on the number of species involved, their
natural hosts, geographic distributions, and basic epidemiology. For 80 years,
this lack of understanding has limited our ability to determine which species
of schistosomes in the U.S. are most responsible for outbreaks, let alone
worldwide. Much of our knowledge of dermatitis in North America is severely out
of date. Most of the diverse clade of avian schistosomes is poorly known
taxonomically and the classification and relationships are ambiguous
or unknown.
Why Trichobilharzia? Compared to the mammal schistosomes, bird schistosomes have
received less attention, especially Trichobilharzia, the largest genus within
Schistosomatidae.
There are reported over 40 species of Trichobilharzia world wide, mostly from ducks.
Parasites of the avian schistosome genus Trichobilharzia are one of the genera responsible
for a common and recurrent ailment, cercarial dermatitis, caused by the
penetration of human skin by the cercariae of non-human schistosome parasites,
in both shallow freshwater and marine habitats worldwide. The avian
schistosomes responsible for dermatitis outbreaks are poorly characterized in
the U.S. and we lack reliable information on the number of species involved,
their natural hosts, geographic distributions, and basic epidemiology. The most
immediate and pervasive problem with respect to understanding
dermatitis-causing schistosomes from the U.S. is that we remain reliant on
dated morphological descriptions to differentiate and enumerate species. We
lack a similar level of understanding of host usage for the most common species
causing dermatitis in freshwater, Trichobilharzia. In many cases, dermatitis-causing
cercariae have been identified from snails without experimental or molecular
verification of the identity of the corresponding adult worms. It is the goals
of this project to use morphology and DNA of both adults and larval stages to
identify the diversity and host use of Trichobilharzia in the U.S.
Swimmer's itch
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Adult worms of Trichobilharzia in ducks release eggs into the
environment where the newly hatch larvae find and penetrate a snail. In the snail,
the worm undergoes many clonal generations until swimming larva are released
into the environment. These infective larvae will complete the life cycle by
penetrating the foot/legs of ducks or geese and develop into adults. This
swimming stage has been the cause of cercarial
dermatitis, or swimmer's itch in people. The adult worms live in the blood
vessels of the intestine in ducks and geese. Because of the remote habitat in
the ducks, their small size and difficulty in identifications, very little is
know about how many species of these worms exist, especially here in North
America. Therefore, more attention is needed towards understanding the
diversity of these worms in nature.
Eggs in feces

There
are three goals for this project:
1) To
collect waterbirds globally to document the species of schistosome, their hosts
and their distributions. Such information will be useful not only to the
general scientific community, but to State Fish and Game departments and
waterfowl groups.
2) To
collect freshwater and marine snails globally to look for avian schistosome
cercariae and try to match those with what we know about the adult worms. To
document the complete life cycle of these worms, we need to know not only the
species of adults we may find in the waterbirds, but also which snails and how
many different kinds, are necessary to complete the life cycle.
3) Once we
have all of this information, we will use the DNA sequence data from these
worms to determine the following;
-What are
the phylogenetic and phylogeographic relationships?
-Do worms
remain in the ducks during migration north and/or south?
or
-Are
worms purged during fall migration, and ducks acquire new infections in the
spring? –or do the worms go into remission during fall/winter, and
commence egg production in the spring when they are in their breeding
grounds?
-Are there
particular genetic groups more prone to cause cercarial dermatitis?
-How many
of the species of Trichobilharzia in North America cause disease in
ducks?
-What is
the distribution of snail host use?
To date we
have examined over 400 birds representing about 50 species and many
individual snails
representing about 25 species and found 15 taxa of avian
schistosomes.
The Schistosome Group Prague has made
significant advances in the systematics and biology of these worms in
Europe.
Collaborators: