Genetic gradient of a host–parasite pair along a river persisted ten years against physical mobility: Baltic Salmo salar vs. Gyrodactylus salaris

Lumme, Jaakko; Anttila, Pasi; Rintamäki, P.; Koski, Perttu; Romakkaniemi, Atso

doi:10.1016/j.meegid.2016.08.006

Cited by 8 publications

(16 citation statements)

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“…Coevolution of hosts and parasites is a familiar concept in the literature (Ehrlich & Raven, ; Thompson, ), and the topics of host–parasite co‐adaptation and co‐extinction are now receiving increasing attention, as loss of species that are interdependent through mutualistic or parasitic interactions may have cascading effects across taxa in ecosystems worldwide (Dunn, Harris, Colwell, Koh, & Sodhi, ; Farrell, Stephens, Berrang‐Ford, Gittleman, & Davies, ; Koh et al, ). Genetic and phenotypic variation related to host–parasite interactions has been observed in terrestrial and aquatic species (Lagrue, Joannes, Poulin, & Blasco‐Costa, ; Mikheyev et al, ), including parasites of certain freshwater fishes (Dallas & Cornelius, ; Lumme, Anttila, Rintamäki, Koski, & Romakkaniemi, ; Raeymaekers, Wegner, Huyse, & Volckaert, ), and is especially well‐studied in plant–insect interactions (Althoff, Segraves, & Johnson, 2014). Relationships among populations of parasites and populations of hosts are complex and may be influenced by local biotic interactions such as competition for hosts or host immune or behavioural response, as well as biophysical properties of the environment (Janz, ; Laine, ; Thompson, ).…”

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confidence: 99%

Geographic variation in host fish use and larval metamorphosis for the endangered dwarf wedgemussel

White

Ferreri

Lellis

et al. 2017

Aquatic Conservation

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1. Host fishes play a crucial role in survival and dispersal of freshwater mussels (Unionoida), particularly rare unionids at conservation risk. Intraspecific variation in host use is not well understood for many mussels, including the endangered dwarf wedgemussel (Alasmidonta heterodon) in the USA.2. Host suitability of 33 fish species for dwarf wedgemussel glochidia (larvae) from the Delaware and Connecticut river basins was tested in laboratory experiments over 9 years. Relative suitability of three different populations of a single host fish, the tessellated darter (Etheostoma olmstedi), from locations in the Connecticut, Delaware, and Susquehanna river basins, was also tested.3. Connecticut River basin A. heterodon metamorphosed into juvenile mussels on tessellated darter, slimy sculpin (Cottus cognatus), and Atlantic salmon (Salmo salar) parr. Delaware River basin mussels metamorphosed using these three species, as well as brown trout (Salmo trutta), banded killifish (Fundulus diaphanus), mottled sculpin (Cottus bairdii), striped bass (Morone saxatilis), and shield darter (Percina peltata). Atlantic salmon, striped bass, and sculpins were highly effective hosts, frequently generating 5+ juveniles per fish (JPF) and metamorphosis success (MS; proportion of attaching larvae that successfully metamorphose) ≥ 0.4, and producing juveniles in repeated trials. In experiments on tessellated darters, mean JPF and MS values decreased as isolation betweenthe mussel source (Connecticut River) and each fish source increased; mean JPF = 10.45, 6.85, 4.14, and mean MS = 0.50, 0.41, and 0.34 in Connecticut, Delaware, and Susquehanna river darters, respectively. Host suitability of individual darters was highly variable (JPF = 2-11; MS = 0.20-1.0). 5.The results show that mussel-host fish compatibility in A. heterodon differs among Atlantic coastal rivers, and suggest that hosts including anadromous Atlantic salmon and striped bass may help sustain A. heterodon in parts of its range. Continued examination of host use variation, migratory host roles, and mussel-fish interactions in the wild is critical in conservation of A. heterodon and other vulnerable mussel species.

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Section: Introductionmentioning

confidence: 99%

Geographic variation in host fish use and larval metamorphosis for the endangered dwarf wedgemussel

White

Ferreri

Lellis

et al. 2017

Aquatic Conservation

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“…G. salaris infected 33% of the sedentary juveniles (parr) and 82% of the sea-migrating juveniles (smolts). The local parr populations were apparently not infected via the migrating adults or smolts, but the infection was maintained in the nursery rapids via transmission between sedentary juveniles aged 0-4 years (Lumme et al 2016a). The older parr were more often infected than the first year fry (Anttila et al 2008).…”

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confidence: 97%

“…The older parr were more often infected than the first year fry (Anttila et al 2008). The smolts arriving at the river mouth still carried parasite clones from home, and parasite exchange was limited even in the crowded smolt trap (Lumme et al 2016a). The conclusion is that spatial genetic differentiation is maintained by local coadaptation of the host and parasite despite the migration of fish from the upper to the lower Tornio River.…”

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confidence: 97%

“…In coastal samples around the North Sea, the cox2 of Gyrodactylus gondae Huyse, Malmberg et Volckaert, 2004, on the goby host Pomatoschistus minutus (Pallas), showed haplotype diversity (h) between 0.624 to 0.784, and the total number of detected haplotypes was 30 (Huyse et al 2017). This is twice the number of known cox1 haplotypes in all known salmon-specific populations of G. salaris (see Lumme et al 2016a).…”

mentioning

confidence: 98%

“…In the large Baltic Tornio River, the population of the parasite G. salaris carried five mitochondrial haplotypes, distributed unevenly in the upper and lower parts of the 460 km transect during ten years of investigation. The spatial differentiation was F ST = 0.534 (Lumme et al 2016a). G. salaris infected 33% of the sedentary juveniles (parr) and 82% of the sea-migrating juveniles (smolts).…”

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Horizontal transmission of the ectoparasite Gyrodactylus arcuatus (Monogenea: Gyrodactylidae) to the next generation of the three-spined stickleback Gasterosteus aculeatus

Lumme

Ziętara

2018

FOLIA PARASIT

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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 differentiation 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 mitochondrial 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 only h = 0.364 (F = 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 of G. salaris Malmberg, 1957, on the Baltic salmon Salmo salar Linnaeus.

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Global parasite trafficking: Asian Gyrodactylus (Monogenea) arrived to the U.S.A. via invasive fish Misgurnus anguillicaudatus as a threat to amphibians

Reyda

Wells

Ermolenko³

et al. 2019

Biol Invasions

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A monogenean flatworm Gyrodactylus jennyae Paetow, Cone, Huyse, McLaughlin & 24 Marcogliese, 2009 was previously described as a pathogen on bullfrog Lithobates 25 catesbeianus Shaw, 1802, in a Canadian captive population originating in Missouri, U.S.A. 26 The ITS barcoding of G. jennyae showed relatedness to Asian Gyrodactylus macracanthus 27 Hukuda 1940, a parasite of the Asian loach Misgurnus anguillicaudatus Cantor, 1842. The 28 resulting suggestion that the globally invasive pet-trade of fish may be a mechanism for 29 arrival of Gyrodactylus species to North America provided the framework for the current 30 study. The present study was undertaken following the discovery of two other species of 31 Gyrodactylus in a population of illegally introduced M. anguillicaudatus in New York State. 32 Here the invasion hypothesis was tested via DNA sequencing of the ITS of the two 33 Gyrodactylus species obtained from M. anguillicaudatus from New York, termed 34 Gyrodactylus sp. A and Gyrodactylus sp. B. Both Gyrodactylus sp. A and Gyrodactylus sp. B 35 were closely related to G. jennyae and G. macracanthus, and all belong to a molecularly well-36 supported monophyletic Asian freshwater group. In conclusion, this invasive fish has 37 trafficked at least three parasite species to the U.S.A., one of them also found on frog. This 38 route from the Asian wetlands to other continents is similar to that of amphibian chytrid fungi 39 of genus Batrachochytrium Longcore, Pessier & Nichols, 1999. 40 41 Keywords 42 Intercontinental parasite dispersal 43 Molecular systematics 44 Aquatic invasive species 45 Chytrid fungus 46 47 4 (2005) estimated that there are 50,000 foreign plant or animal species in the United States 73 alone, and that 42% of endemic species are endangered or threatened because of aliens. The 74 authors concluded that the total economic damages and losses caused by invasive species add 75 up to an estimated $120 billion per year in the U.S.A. alone. 76 This study maps a complex case of an introduced and rapidly spreading Asian fish in 77 North America, accompanied by East Asian parasites. The starting point of this narrative was 78 as follows. A monogenean flatworm species Gyrodactylus jennyae Paetow, Cone, Huyse, 79 McLaughlin and Marcogliese 2009 was described as a new pathogenic parasite on the 80 American bullfrog Lithobates catesbeianus Shaw, 1802 in North America. The bullfrog itself 81 is widely trafficked (Mata-López et al. 2010). Paetow et al. (2013) also demonstrated that G. 82 jennyae infection increased the mortality of the tadpoles associated with fungal disease 83 Batrachochytrium dendrobatidis Longcore, Pessier & Nichols, 1999, making matters worse. 84 This fungal disease is considered one of the main reasons for the contemporary decline of 85 global amphibian populations (Collins and Crump 2009). The question was raised about the 86 origin of this newly described Gyrodactylus species, which are monogenean ectoparasites of 87 fish, seldom found on amphibians. Records on amphibians were reviewed in P...

show abstract

Genetic gradient of a host–parasite pair along a river persisted ten years against physical mobility: Baltic Salmo salar vs. Gyrodactylus salaris

Cited by 8 publications

References 20 publications

Geographic variation in host fish use and larval metamorphosis for the endangered dwarf wedgemussel

Geographic variation in host fish use and larval metamorphosis for the endangered dwarf wedgemussel

Horizontal transmission of the ectoparasite Gyrodactylus arcuatus (Monogenea: Gyrodactylidae) to the next generation of the three-spined stickleback Gasterosteus aculeatus

Global parasite trafficking: Asian Gyrodactylus (Monogenea) arrived to the U.S.A. via invasive fish Misgurnus anguillicaudatus as a threat to amphibians

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