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Horizontal Transmission of the Ectoparasite Gyrodactylus

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Horizontal Transmission of the Ectoparasite Gyrodactylus B6!!DD 6!;2E1<+22< doi: E2E99EEF;2E122< http://folia.paru.cas.cz Research Article Horizontal transmission of the ectoparasite Gyrodactylus arcuatus (Monogenea: Gyrodactylidae) to the next generation of the three-spined stickleback Gasterosteus aculeatus Jaakko LummeE and B; E !#"G= ; !"#L%6 In the parthenogenetic monogeneans of the genus Gyrodactylus HE15;7!'7@' hosts is determined by the relative roles of lateral transmission and clonal propagation. Clonality and limited transmission lead to 7!73!!B773%@%Gasterosteus aculeatus Linnaeus, the local mitochondrial diversity of Gyrodactylus arcuatus7'%E-557!7ƽ3 '%K7!77>! %@%'!7@%7'M!NNNcox1513 77'[B!7!7'7!777 (h) was >ƽ@'[7'!!@Q hR2-;<h = 2-51SBG@9<U7V sticklebacks carried G. arcuatusK7@![7'6@2-;/E29Q/S G@;';51/+22G@;+K77V' as high as in adults (hR2-E<S@7[7'hR25<9QFSTR2<2S' !K7[[!7[!'@!7 host adulthood via continuous transmission. Nesting and polygamy are suggested as factors maintaining the high genetic diversity of 7K7M7G. arcuatus is fundamentally ƽ7G. salaris@!E-+N7Salmo salar Linnaeus. clonal propagation, competition, parasite transition K7!QEM9S7FF*FF;2E13<+322< Some important aspects of the population genetics and ten overcome by having a very large number of random3 ƽ ly spread propagules. The main characteristics of the host 7 3! ! K7 3 which determine the metapopulation structure and the namics among demes on single hosts in many parasite strategy of the parasite are: (i) the carrying capacity of !@>7M !777*=QS7!3 of host generations and randomness in the transition pro3 ity of the host, relative to the turnover rate of the parasite cess. The hosts represent ephemeral resource units. If the Q7S=QS7 parasite is not vertically transmitted, the new host genera3 77=QS776 tion is born uninfected, and the parasites have – actively or factors which determine metapopulation structure and par3 passively – to locate and infect new host individuals. The asite strategy include the dispersal capacity and length of death of a host means the end of the resource patch. The the dispersal phase of the parasite. The parasites often have transition between host generations is critical, and the life 7>@'>! cycle of the parasite should be adapted to this transition. The simple and direct transmission biology of hyper3 7'773 viviparous, parthenogenetic and hermaphroditic mono3 3!%7[3 ! \' 7 ! Gyrodactylus Nordmann, !F@Q7ZE-<9S E15;''@!. Q;22+S' K77![!@'73 D755%%Q;22NSGyrodactylus para3 B!"#L%&'*+-123521 #L%667891+1+;5<2+2=>891+1+;5<22;=3%*?@! This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. E2E99EEF;2E122< Z]*Gyrodactylus arcuatus @'3 K7xV%%Gyrodactylus arcuatus 3 Q%%;22;;22NSK7!73 7'%E-55751cox1 @ 3!' 77ƽ@'xV%% QD@];22;SK77 H;N2%'!!@ 7[7 QST R22EEZ;2E<@SK7ƽ@3 K7!7!373 served between G. salaris and G. arcuatus or G. gondae distinct phases for dispersal or dormancy but, at any time @ > @ ƽ! 7 3 during their life, the worms are able to switch from one @ 7 ƽ! 77Q!;22+S 73! G 7 ! M 7 3 ]'@ tance of transmission between host individuals and/or the transmission of G. arcuatus7>! generations, and the clonal propagation of gyrodactylids. host in the wild. In the brackish water coastal habitats of In the Gyrodactylus model, the transmission is direct, but 7773%@%QGasterosteus @M 7! ! aculeatus Linnaeus) forms dense and continuous popula3 [ 7!7 3 QD;221;2E5SB[ M ! parasite G. arcuatus is also common and numerous, as well > Gyrodactylus salaris Malmberg, @!!Q;221Z E-+NSalmo salar Linnae3 ;2E<@S77!77 us, the populations were strongly structured, apparently by of the parasite, transmission can be studied at the level of !Q_;22-SB77 7& ' 7' 7 7 @' salmon spawning rivers in the great lake basins of Onega host generations may present a model for studying the pop3 and Ladoga in Russian Karelia, only one parasite mito3 ulation dynamics of the parasite, which is important for un3 chondrial haplotype was observed. There is no transmis3 !77733 sion between adults feeding in the open lakes. The parasite K773%@%@ @V77 !Q!7;222@;2E5S 7@ƽ Studies of the parasites, which have a shorter generation B7!Kq77 time, might also add an interesting dimension to the under3 parasite G. salaris[77 !7@!77QD;22+= distributed unevenly in the upper and lower parts of the ];22+=Z;2E<@S 9<2%!!K73 ƽ'FSTR2+59QZ;2E<S MATERIALS AND METHODS G. salaris55U7VQS The parasite material investigated here was partly utilised for 1;U73!!VQSK7 other purposes earlier. The global population structure and phy3 parr populations were apparently not infected via the mi3 logeography of Gyrodactylus arcuatus was previously reported grating adults or smolts, but the infection was maintained QZ;2E<@SB77xV%%' in the nursery rapids via transmission between sedentary V'7! V!2M9QZ;2E<SK7 hosts. The details of the genetic structure among old and young '77[Q3 777>!3 ;221SK7!77 eration of sticklebacks is reported here. Knowing the details also 7>7! provides an important lesson for parasite sampling: fewer adults was limited even in the crowded smolt trap (Lumme et al. 7V7!7 ;2E<SK77!ƽ3 local genetic diversity. tion is maintained by local coadaptation of the host and 7![777 ! lower Tornio River. %@%Q[77GZ!7+NM<E B![773 HR59S'77@!;< ty for genetic migration between populations allows these ! ;229 xV%% 7 Q<9-;E5H= parasites to reach populations which are an order of mag3 ;+E2E-S777! !777'[7DM were postreproductive, under a heavy parasite load, often swim3 7! > @ 7!7 B !7>@@ samples around the North Sea, the cox2 of Gyrodactylus 7>77Schistocephalus DE1;- gondae]@!x%;2297!@ The parasite load included thousands of Gyrodactylus covering host Pomatoschistus minutus Q6S 7' 7 77[7Q!ES7 diversity (hS@'2<;92N197@ Schistocephalus solidusQENN<S7@7@3 7'52Q];2ENSK7 valve glochidia in the skin, and the crustacean Argulus foliaceus twice the number of known cox1 haplotypes in all known ZEN+17Q]S7% 3[G. salaris (see Lumme et HM77'3 ;2E<S tempted. A sample of G. arcuatusQHR;2S[7 6!;2E1<+22< 6!;1 E2E99EEF;2E122< Z]*Gyrodactylus arcuatus --5E-5M--5E-+ ";;5;9< "5291;+ _K599E;9M _K599E;<S Gyrodactylus turnbulli ]E-1<M! Poecilia reticulata 6 6 ' 7 ! 10 mm H ' @ !! ! E2)@ƽQE&6Dq@ƽ29+UQFSK';229+U QFSH692<23!F_SK7@'@3 5 mm <+D;+'_!7 -+DE277 9DM;37' 6Dq[ K7;2)6Dq>E& 6Dq@ƽ2;HK6;!D;E)7 2+"KMHQxZ7S ;)!K7!['-9D5 51-9D for 40 s, +2D52N;DE+ [>N;DN. K7 BK H % 7 [ ' [ '7 BKE Q+3KKKDD#K##K# DDK35SBK;qQ+3##KKDD#DKK#KD35S ' M '7 BKEq Q+3KKK#D#KKD###D3 D#35S BK; Q+3K##K##KDDKD##DKD35S3 Fig. 1.6 Gasterosteus aculeatus Linnaeus H;[7'!7!@Gyrodac- [Q;221SK7 tylus arcuatus7'%E-55'!@7 M'#%Q99+-9;S >! 7 H QE<22 ! cox1) was am3 [ '7 D>< Q+3KK##KDK#D#DK##KK35S E<q Q+3DKKKKDK#K#D##35S 3 H;N2%7!7''77 Q;2E2SK7ZE xV%% Q+3KK######KKK##K35S D>N Q+3KKKKDK3 K7 [ V [7 Q[7 7 G"H# !7 ##KK##D#K35S qD>; Q+3K##DK##3 E1M;NHR<-S'77 D#DDD35S'M!K7M' xV%%[7'%-<U73 #%Q99<N<NS K7 [7 ' !7 ; G@ ;229 Q[7 !7 K7 M ! ' @ D& 3 E1M;5S'7+9UK7[7 7#9%!QK;229;22NS 77K7V[7 7V7[!7NNNK77! '%7'%;+G@;229B3 '@H!7@!7@> ;9V!7E-M;NB7 Composite Likelihood distances (dMCL), correcting upwards the 7'9;U large distances reaching saturation. The bootstrap test was con3 B7Q+S7'3 '7E222' M7[7Q5+!7S@7V [ ! QN5 !7S ' [ @ 7 NNN77QZ;2E<@S " &7 The randomness of the numeric parasite distributions on Q7R>! 7 V [7 ' '7 6 @ Q;17R@@!7>Q Q>R;RRS@3F = s;F> 7;1R dfER3E;R.K7@7' ; 7RHFQH3ESQE3 SK7[>>FST based "# 7M'FST = (hT-hS)/hT, where K7@!7NNN!7H hT is the total diversity and hS is the mean diversity in separate was conducted and the global mitochondrial variation was report3 K7ZST'777ƽ QZ;2E<@SK77!77 was estimated by ǓǍdžǒǖNJǏ5EK7@73 xV%%[EK7[ lotype diversity (hSQ4S 7xV%%7[;#%3 QKVRDRFs) were also calculated using ǓǍdžǒǖNJǏ5E @MG. arcuatusQ2N1N2EM Q>ƾ;22+S 2N1NE-"1<;<1EM"1<;N29SG. lucii Kulakovskaya, K7>@73 E-+;Q99<N9-M99<N+N"5291ENM"5291;9SG. sal- lotypes drawn randomly from the base population (null model), arisQ9N-N+2+921-E+921-;+921--+92-2E !''Q +92-25 +92-2+ +92-2< EEN11- 9-+2<5 [5S'77@ +N2E;2 <E;9<9 9N;219 9N;21+ 192;;; '7H7MxV%% E12555 9<1E;1 -11-5E --5E1- --5E-E GZG"H#K777'77' 6!;2E1<+22< 6!51 E2E99EEF;2E122< Z]*Gyrodactylus arcuatus Table 1.]Gyrodactylus arcuatus7'% arisQ77!77!S@ƽ7 E-55xV%% of G. lucii. BK@;7H77[73 ] GZ G"H# G'7GZ E E 3 77[7'@G. arcuatus ; < N A4 E 5 Q!ES7'@ N E 3 sample for global phylogeographic analysis. 1 E 3 The parasite sample separately counted from the seven - N 1 [7;+!77 E2 3 ; ' 7 ! [7 7 EE E 3 E; E 3 7![7K7 E9 E 3 GZ E- 7 E+ '77 ' 3 E+ 3 E gletons (present as one individual). The other four hap3 E< E 3 ' @ ; 9 < N EN E 3 7[7QK@;S@3 E1 4 E9 E- E E QHR;2=Z;2E<@S[7H ;5 3 5 ;N2 % 7 ! 7 E1 ! ;9 3 ; and only one haplotype pair.
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