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Horizontal Transmission of the Ectoparasite Gyrodactylus Arcuatus

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Horizontal Transmission of the Ectoparasite Gyrodactylus Arcuatus Institute of Parasitology, Biology Centre CAS Folia Parasitologica 2018, 65: 006 doi: 10.14411/fp.2018.006 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 Lumme1 and Marek S. Ziętara2 1 Department of Ecology and Genetics, University of Oulu, Finland; 2 Faculty of Biology, University of Gdańsk, Poland Abstract: In the parthenogenetic monogeneans of the genus Gyrodactylus Nordmann, 1832, the genetic diversity within or between hosts is determined by the relative roles of lateral transmission and clonal propagation. Clonality and limited transmission lead to high-amplitude metapopulation dynamics and strong genetic drift. In Baltic populations of the three-spined stickleback Gasterosteus aculeatus Linnaeus, the local mitochondrial diversity of Gyrodactylus arcuatus Bychowsky, 1933 is very high, and spatial differentia- tion weak. To understand the transmission dynamics in a single location, the transmission of the parasite from adults to next generation sticklebacks was investigated in a northern Baltic brackish water location. By sequencing 777 nt of cox1, as many as 38 separate mito- chondrial haplotypes were identified. In August, the intensity of gyrodactylid infection on adult hosts was high, the haplotype diversity (h) was extreme and differentiation between fish was negligible (total h = 0.926, mean h = 0.938). In October, only 46% of the juvenile sticklebacks carried G. arcuatus. The number of parasites per young fish followed a Poisson distribution 0.92 ± 1.04 (mean ± SD) on October 2, and was clearly overdispersed 2.38 ± 5.00 on October 25. The total haplotype diversity of parasites on juveniles was nearly as high as in adults (h = 0.916), but the mean per fish was onlyh = 0.364 (FST = 0.60), due to low intensity of infection and rapid clonal propagation of early arrivals. The initial first come first served advantage of the first gyrodactylid colonisers will be lost during the host adulthood via continuous transmission. Nesting and polygamy are suggested as factors maintaining the high genetic diversity of the parasite population. The transmission dynamics and, consequently, the population structure of Baltic G. arcuatus is fundamentally different from that ofG. salaris Malmberg, 1957, on the Baltic salmon Salmo salar Linnaeus. Keywords: clonal propagation, competition, parasite transition This article contains supporting information (S1–S4) online at http://folia.paru.cas.cz/suppl/2018-65-006.pdf Some important aspects of the population genetics and ten overcome by having a very large number of random- evolution of parasites are fundamentally different from ly spread propagules. The main characteristics of the host those of free-living organisms. The metapopulation dy- 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 groups can be extreme, due to the complicated sequence a single host specimen, i.e. the patch size; (ii) the longev- of host generations and randomness in the transition pro- ity of the host, relative to the turnover rate of the parasite cess. The hosts represent ephemeral resource units. If the (patch duration); (iii) the spatial and temporal distance of parasite is not vertically transmitted, the new host genera- the host individuals; and (iv) the host immunity. Parasitic tion is born uninfected, and the parasites have – actively or factors which determine metapopulation structure and par- 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 a phase of asexual multiplication between sexual stages. cycle of the parasite should be adapted to this transition. The simple and direct transmission biology of hyper- From the point of view of the parasite, some hosts rep- viviparous, parthenogenetic and hermaphroditic mono- resent coarse-grained and risky resources, others are fine- genean flatworms of the genus Gyrodactylus Nordmann, grained and/or predictable (MacArthur and Levins 1964). 1832 was well outlined by Boeger et al. (2005), as well as The challenge of finding a suitable new host is most of- in Chapter 3.3 in Bakke et al. (2007). Gyrodactylus para- Address for correspondence: M.S. Ziętara, Department of Molecular Evolution, Faculty of Biology, University of Gdańsk, ul. Wita Stwosza 59, 80-308 Gdańsk, Poland. Phone: +48 58 523 60 50; Fax: +48 58 523 60 02; E-mail: [email protected] 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. doi: 10.14411/fp.2018.006 Lumme and Ziętara: Horizontal transmission of Gyrodactylus arcuatus sites are intermediate between micro- and macroparasites The Varjakka population of Gyrodactylus arcuatus By- (Bakke et al. 2002, 2007). The progeny of these ectopar- chowsky, 1933 analysed here carried as many as 38 cox1 asites are born as full-grown individuals, one at a time haplotypes, and the differentiation between Varjakka and (Cable and Harris 2002). Their hyperviviparity sets strict Närpiö populations situated 270 km apart was negligible limits to the dispersal capacity and defines the life cycle. (ΦST = 0.011, Lumme et al. 2016b). The differences ob- The straight single-host, adult-only life cycle contains no served between G. salaris and G. arcuatus or G. gondae distinct phases for dispersal or dormancy but, at any time may be explained by differing connectivities of the par- during their life, the worms are able to switch from one asite populations caused by their differing capacities for host individual to another (Boeger et al. 2005). host-dependent migration. One of the remaining questions is the relative impor- Here, we introduce and test an amenable system to study tance of transmission between host individuals and/or the transmission of G. arcuatus to the next generation of 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 the Baltic Sea, the three-spined stickleback (Gasterosteus subsequent parthenogenetic clonal propagation may lead aculeatus Linnaeus) forms dense and continuous popula- to amplified metapopulation dynamics, high clonal rar- tions (Cano et al. 2008, DeFaveri et al. 2013). Its specific efaction and consequential loss of genetic variation. For parasite G. arcuatus is also common and numerous, as well example, in a study of Gyrodactylus salaris Malmberg, as being genetically diverse (Ziętara et al. 2008, Lumme et 1957, a parasite of Atlantic salmon Salmo salar Linnae- al. 2016b). Due to the high local mitochondrial diversity us, the populations were strongly structured, apparently by of the parasite, transmission can be studied at the level of genetic drift (Kuusela et al. 2009). In each of the isolated haplotypes. We will show that the transmission between salmon spawning rivers in the great lake basins of Onega host generations may present a model for studying the pop- and Ladoga in Russian Karelia, only one parasite mito- ulation dynamics of the parasite, which is important for un- chondrial haplotype was observed. There is no transmis- derstanding the evolution and coevolution of the host-para- sion between adults feeding in the open lakes. The parasite site system. The three-spined stickleback is a superb model populations are maintained by various juvenile cohorts that for studying evolution (e.g. Schluter 2000, Barber 2013). inhabit different rivers. Studies of the parasites, which have a shorter generation In the large Baltic Tornio River, the population of the time, might also add an interesting dimension to the under- parasite G. salaris carried five mitochondrial haplotypes, standing of the biology of the host (Criscione et al. 2005; distributed unevenly in the upper and lower parts of the Huyse et al. 2005; Lumme et al. 2016b). 460 km transect during ten years of investigation. The spa- tial differentiation was FST = 0.534 (Lumme et al. 2016a). MATERIALS AND METHODS G. salaris infected 33% of the sedentary juveniles (parr) The parasite material investigated here was partly utilised for and 82% of the sea-migrating juveniles (smolts). The local other purposes earlier. The global population structure and phy- parr populations were apparently not infected via the mi- logeography of Gyrodactylus arcuatus was previously reported grating adults or smolts, but the infection was maintained (Lumme et al. 2016b). In that paper, the Varjakka material was in the nursery rapids via transmission between sedentary presented as just one population, without specifying individual juveniles aged 0–4 years (Lumme et al. 2016a). The older hosts. The details of the genetic structure among old and young parr were more often infected than the first year fry (Antti- host individuals, and the transmission from adults to the next gen- la et al. 2008). The smolts arriving at the river mouth still eration of sticklebacks is reported here. Knowing the details also carried parasite
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