Diversity and Ancestry of Flatworms Infecting Blood of Nontetrapod

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From: Raphael Orélis-Ribeiro, Cova R. Arias, Kenneth M. Halanych, Thomas H.
Cribb, Stephen A. Bullard, Diversity and Ancestry of Flatworms Infecting Blood of
Nontetrapod Craniates “Fishes”. In D. Rollinson, J. R. Stothard
editors: Advances In Parasitology, Vol. 85,
Oxford: United Kingdom, 2014, pp. 1-64.
ISBN: 978-0-12-800182-0
© Copyright 2014 Elsevier Ltd
Academic Press
Author's personal copy
CHAPTER ONE
Diversity and Ancestry of
Flatworms Infecting Blood of
“ ”
Nontetrapod Craniates Fishes
* † {
Raphael Orélis-Ribeiro , Cova R. Arias , Kenneth M. Halanych ,
Thomas H. Cribb}, Stephen A. Bullard*,1
*
AquaticParasitologyLaboratory,SchoolofFisheries,AquacultureandAquaticSciences,Collegeof
Agriculture,AuburnUniversity,Auburn,Alabama,USA
†AquaticMicrobiologyLaboratory,SchoolofFisheries,AquacultureandAquaticSciences,Collegeof
Agriculture,AuburnUniversity,Auburn,Alabama,USA
{DepartmentofBiologicalSciences,AuburnUniversity,Auburn,Alabama,USA
}SchoolofBiologicalSciences,TheUniversityofQueensland,Brisbane,Queensland,Australia
1Correspondingauthor:e-mailaddress:[email protected]
Contents
1. Introduction 2
2. LifeHistory 34
3. Taxonomy 39
4. Phylogeny 41
5. ApproachtoOurPhylogeneticAnalysis 45
6. ResultsfromOurPhylogeneticAnalysis 48
7. SummaryofPhylogeneticStudy 50
8. FutureDirections 53
Acknowledgements 55
References 55
Abstract
Wehereinreviewallpublishedmolecularstudies(lifehistory,taxonomy,andphylog-
eny)andsummarizeallGenBanksequencesandprimersetsforthe“fishbloodflukes”.
Further,byanalysingnewandallavailablesequencedataforthepartialD1–D2domains
of 28S from 83 blood fluke taxa, we explore the evolutionary expansion of flatworm
parasitisminthebloodofcraniates.Basedonthisanalysis,thebloodflukesinfecting
marine bony fishes (Euteleostei) are monophyletic. The clade comprising the
chondrichthyanbloodflukeplusthemarineeuteleostbloodflukesisthesistergroup
totetrapodbloodflukes(spirorchiidsandschistosomes).Theinnominatebloodfluke
cercariaefromfreshwatergastropodsweremonophyleticandsistertothecladecom-
prisingspirorchiidsandschistosomes,butlownodalsupportindicatedthattheymay
representadistinctbloodflukelineagewithphylogeneticaffinitiesalsotofishblood
flukes. Blood flukes that utilize gastropod intermediate hosts were monophyletic
AdvancesinParasitology,Volume85 #2014ElsevierLtd 1
ISSN0065-308X Allrightsreserved.
http://dx.doi.org/10.1016/B978-0-12-800182-0.00001-5
Author's personal copy
2 RaphaelOrélis-Ribeiroetal.
(unidentifiedgastropodcercariae+tetrapodbloodflukes)andthoseutilizingbivalves
and polychaetes were monophyletic (marine fish blood flukes). Low or no taxon
samplingamongbloodflukesofbasalfishlineagesandprimarydivisionfreshwaterfish
lineages are significant data gaps needing closure. We also note that no record of
an infection exists in a hagfish (Myxiniformes), lamprey (Petromyzontiformes), or
nontetrapod sarcopterygiian, i.e., coelacanth (Coelacanthimorpha) or lungfish
(Dipnoi). The present phylogenetic analysis reiterated support for monophyly of
Schistosomatidaeandparaphylyofspirorchiids,withthebloodflukesoffreshwatertur-
tlesbasaltothoseofmarineturtlesandschistosomes.
1. INTRODUCTION
Blood flukes (Platyhelminthes: Digenea: Schistosomatoidea) histori-
cally have been assigned to three families, each corresponding to the
vertebrate definitive host lineages they infect (Amemiya et al., 2013;
Nelson, 2006). Fish blood flukes (Digenea: Aporocotylidae; also as
“Sanguinicolidae”; hereafter referred to as “FBFs”) (Bullard et al., 2009;
Smith,1972,1997a,b,2002)infectnontetrapodcraniates,i.e.,paraphyletic
fishes. Turtle blood flukes (Digenea: paraphyletic “Spirorchiidae”) princi-
pally infect marine and freshwater turtles (Chelonia) (Snyder, 2004), with
recent molecular phylogenetic support for inclusion of the crocodile-
infecting, dioecious blood fluke Griphobilharzia amoena (see Brant and
Loker,2005;LokerandBrant,2006;Plattetal.,1991,2013).Schistosomes
(Digenea: Schistosomatidae) (see Lockyer et al., 2003b) infect birds and
mammals(Cribbetal.,2001;Olsonetal.,2003)andhavebeenthemoststud-
ied,makingthemamongthebestknownoftrematodefamilies(Brantetal.,
2006). They cause human schistosomiasis and are among the world’s most
economically important metazoan parasites, with the species of Schistosoma
(principallyS.mansoni,S.japonicum,andS.haematobium)infecting>230mil-
lionpeoplefrom28countriesandkillinganestimated280,000peopleannu-
allyinsub-SaharanAfrica(Rollinsonetal.,2013;VanderWerfetal.,2003;
WorldHealthOrganization,2010).Mostphylogeneticattentionhasfocused
onschistosomes,andabundantevidenceexiststhattheycompriseamono-
phyletic group. Two molecular phylogenetic studies have been published
forturtlebloodflukes(Snyder,2004;Tkachetal.,2009)andnineforthoseof
FBFs.Thelatteranalysestypicallyincludealimitednumberoftaxaandmarkers
(Tables 1.1–1.3) and treat relationships between or within genera, natural
history, or life cycles (Aiken et al., 2007; Alama-Bermejo et al., 2011;
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Table1.1 GenBankDNAsequencesforfishbloodflukes
GenBankaccessionnumbers
Parasite Host Stage Locality Setting 18S 28S ITS2 COI Reference(s)
Acipensericola Polyodon A Mississippi Wild DQ534192a Bullard et al.
petersoni spathula Delta, the (2008)
United States
Ankistromeces Siganus A SW Pacific, off Wild DQ335838b Nolan and
dunwichensis fuscescens North Cribb(2006a)
Stradbroke
Island, Australia
Ankistromeces Meuschenia A SW Pacific, Wild DQ335839b Nolan and
mariae freycineti off Stanley Cribb(2006a)
Harbour,
Australia
Ankistromeces Siganus A SW Pacific, off Wild DQ335840b Nolan and
olsoni fuscescens Heron Island, Cribb(2006a)
Australia
Aporocotyle Merluccius A SW Atlantic, off Wild JX094803c Herna´ndez-
argentinensis hubbsi Patagonia, Orts et al.
Argentina (2012)
Aporocotyle Genypterus A SW Atlantic, off Wild JX094801a JX094802c Herna´ndez-
mariachristinae blacodes Patagonia, Orts et al.
Argentina (2012)
Continued
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Table1.1 GenBankDNAsequencesforfishbloodflukes—cont'd
GenBankaccessionnumbers
Parasite Host Stage Locality Setting 18S 28S ITS2 COI Reference(s)
Aporocotyle Merluccius A NE Atlantic Wild AF167094c Snyder and
spinosicanalis merluccius Loker (2000)
A NEAtlantic,the Wild AJ287477b Cribb et al.
United (2001)
Kingdom
A NE Atlantic, off Wild AY222177c Olson et al.
Orkney Islands, (2003)
the United
Kingdom
Braya jexi Scarus A SW Pacific, off Wild DQ059624b Nolan and
frenatus Heron Island, Cribb
Australia (2006b)
Braya psittacus Scarus A SW Pacific, off Wild DQ059625b Nolan and
ghobban Heron Island, Cribb
Australia (2006b)
Braya yantschi Chlorurus A SW Pacific, off Wild DQ059628b Nolan and
microrhinos Heron Island, Cribb
Australia (2006b)
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Cardicola aurata Sparusaurata A Mediterranean Cultured AM910616c AM910617b Holzer et al.
Sea, off (2008)
Valencia, Spain
Cardicola bartolii Siganus A SW Pacific, off Wild DQ059631b Nolan and
lineatus Heron Island, Cribb
Australia (2006b)
Cardicola Chaetodon A SW Pacific, off Wild KF049000b Yong et al.
chaetodontis aureofasciatus Lizard Island, (2013)
Australia
Chaetodon E SW Pacific, off Wild KF049004b Yong et al.
baronessa Lizard Island, (2013)
Australia
Chaetodon E SW Pacific, off Wild JN418931b Yong et al.
kleinii Heron Island, (2013)
Australia
Chaetodon E SW Pacific, off Wild KF049002b Yong et al.
lunulatus Lizard Island, (2013)
Australia
Chaetodon E SW Pacific, off Wild KF049003b Yong et al.
plebeius Lizard Island, (2013)
Australia
Continued
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Table1.1 GenBankDNAsequencesforfishbloodflukes—cont'd
GenBankaccessionnumbers
Parasite Host Stage Locality Setting 18S 28S ITS2 COI Reference(s)
Chaetodon A SW Pacific, off Wild JN418932b Yong et al.
rainfordi Heron Island, (2013)
Australia
Chaetodon E SW Pacific, off Wild DQ059633b Nolan and
unimaculatus Heron Island, Cribb
Australia (2006b)
Chaetodon E SW Pacific, off Wild KF049001b Yong et al.
unimaculatus Lizard Island, (2013)
Australia
Cardicola coeptus Siganus A SW Pacific, off Wild DQ059629b Nolan and
punctatus Heron Island, Cribb
Australia (2006b)
A SW Pacific, off Wild JF803976c Cribb et al.
Heron Island, (2011)
Australia
Cardicola coeptus Siganus A SW Pacific, off Wild DQ059630b Nolan and
vulpinus Heron Island, Cribb
Australia (2006b)
A SW Pacific, off Wild JF803977c Cribb et al.
Heron Island, (2011)
Australia
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Cardicola Siganus A SW Pacific, off Wild DQ059634b Nolan and
covacinae punctatus Heron Island, Cribb
Australia (2006b)
Cardicola currani Sciaenops A Gulf of Mexico, KJ272524c Present study
ocellatus offDavisBayou,
the United
States
Cardicola forsteri Longicarpus C SW Pacific, off Wild JF800668c JF800670b Cribb et al.
modestus Port Lincoln, (2011)
S Australia
Cardicola forsteri Thunnus A SW Pacific, off Cultured DQ059637b Nolan and
maccoyii S Australia Cribb
(2006b)
A SW Pacific, off Cultured EF653387c EF661575b Aiken et al.
Port Lincoln, (2007)
S Australia
A SW Pacific, off Wild EF653389c EF653394b Aiken et al.
Cabbage Patch, (2007)
Australia
A SW Pacific, off Cultured AB742426c AB742428b Shirakashi
Port Lincoln, et al. (2013)
S Australia
Continued
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Table1.1 GenBankDNAsequencesforfishbloodflukes—cont'd
GenBankaccessionnumbers
Parasite Host Stage Locality Setting 18S 28S ITS2 COI Reference(s)
Cardicola forsteri Thunnus A Mediterranean Cultured EF653388c EF653395b Aiken et al.
thynnus Sea, off Puerto (2007)
de Mazarro´n,
Spain
Cardicola lafii Siganus A SW Pacific, off Wild DQ059639b Nolan and
fuscescens Lizard Island, Cribb
Australia (2006b)
Cardicola milleri Lutjanus A SW Pacific, off Wild DQ059640b Nolan and
bohar Lizard Island, Cribb
Australia (2006b)
Cardicola Thunnus A NW Pacific, Cultured HQ324227c HQ324228b Ogawa et al.
opisthorchis orientalis Japan (2011)
Cardicola Terebella sp. C NW Pacific, off Wild AB829900c AB830082b Sugiharaetal.
opisthorchis Tsushima, Japan (2014)
Cardicola Thunnus A SW Pacific, off Cultured AB742425c AB742427b Shirakashi
orientalis maccoyii Port Lincoln, et al. (2013)
S Australia
Cardicola Thunnus A NW Pacific, off Cultured HQ324225c HQ324226b Ogawa et al.
orientalis orientalis Kushimoto, (2011)
Japan
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Cardicola palmeri Pogonias A Gulf of Mexico, KJ572525c Present study
cromis off Back Bay,
the United
States
Cardicola parilus Siganus A Indian, off Wild DQ059638b Nolan and
fuscescens Ningaloo Reef, Cribb
W Australia (2006b)
Cardicola Siganus A Indian, off Wild DQ059642b Nolan and
tantabiddii fuscescens Ningaloo Reef, Cribb
W Australia (2006b)
Cardicola Siganus A SW Pacific, off Wild DQ059643b Nolan and
watsonensis corallinus Lizard Island, Cribb
Australia (2006b)
Chimaerohemecus Chimaera A NE Atlantic, off Wild AY157213a AY157239a AY157185a Lockyer et al.
trondheimensis monstrosa Bergen, (2003b)
Norway
Elaphrobates Lutjanus A Gulf of Mexico, KJ572526c Present study
euzeti campechanus USA
Neoparacardicola Naso A SW Pacific, off Wild AY222097a AY222179c Olson et al.
nasonis unicornis Lizard Island, (2003)
Australia
Continued