Host-specific monogeneans parasitizing freshwater fish: The ecology and evolution of host-parasite associations.

Monogenea (Platyhelminthes), mainly gill and fin ectoparasites of fish, are often recognized as host specific and morphologically and ecologically diverse. These parasites exhibit high species diversity at the level of host species or individual fish specimens. Using case studies, especially those widely performed in Dactylogyrus parasitizing cyprinoid fish, this article presents current knowledge on the ecology and evolution of congeneric gill monogeneans. The important aspects of the ecology of congeneric monogeneans are highlighted, in particular: host specificity expressed at several host levels (from strict specificity to phylogenetic specificity), microhabitat specificity expressed by restricted positions on fish gills to facilitate intraspecific mating, and the link between microhabitat preference and morphological adaptation (i.e., sclerotized structures of the haptor) or reproductive isolation. From the evolutionary perspective, this study focused on the processes of the speciation and diversification of congeneric monogeneans, highlighting the role of host switch as the most prominent coevolutionary event, accompanied in some cases mostly by intrahost speciation or cospeciation, as revealed by cophylogenetic studies. Here, important knowledge on evolutionary patterns of host specificity, microhabitat specificity, and morphological adaptation is presented. Host-specific monogeneans may represent an important tool for studying the historical biogeography of their hosts. Specifically, in the case of freshwater fish hosts exhibiting disjunctive distribution, they reflect both historical and contemporary contacts. The role of host-specific congeneric monogeneans in revealing historical intercontinental and intracontinental contacts between freshwater fish is highlighted. Finally, the importance of the role of genetic coadaptation, limiting the presence of host-specific monogeneans in hybrid fish, is emphasized.

Title: Monogènes spécifiques à leur hôte parasitant les poissons d'eau douce : écologie et évolution des associations hôtes-parasites. Abstract: Les Monogènes (Plathelminthes), principalement ectoparasites des branchies et des nageoires des poissons, sont souvent reconnus comme spécifiques à leur hôte et diversifiés morphologiquement et écologiquement. Ces parasites présentent une grande diversité d'espèces au niveau des espèces hôtes ou des spécimens individuels de poissons. À l'aide d'études de cas (en particulier celles largement réalisées chez les Dactylogyrus parasitant les poissons cyprinoïdes), les connaissances actuelles sur l'écologie et l'évolution des monogènes branchiaux congénères sont présentées. Les aspects importants de l'écologie des monogènes congénères sont mis en évidence, en particulier la spécificité à l'hôte exprimée à plusieurs niveaux de l'hôte (de la spécificité stricte à la spécificité phylogénétique), la spécificité du microhabitat exprimée par des positions restreintes sur les branchies des poissons pour faciliter l'accouplement intraspécifique, et le lien entre la préférence du microhabitat et l'adaptation morphologique (c'est-à-dire les structures sclérifiées du hapteur) ou l'isolement reproductif. Du point de vue évolutif, l'étude a été concentrée sur les processus de spéciation et de diversification des monogènes congénères, soulignant le rôle du changement d'hôte comme l'événement coévolutif le plus important, accompagné surtout dans certains cas de spéciation ou de cospéciation intra-hôte, comme le révèlent les études cophylogénétiques. Des connaissances importantes sont présentées ici sur les modèles évolutifs de spécificité d'hôte, de spécificité de microhabitat et d'adaptation morphologique. Les monogènes spécifiques à l'hôte peuvent représenter un outil important pour étudier la biogéographie historique de leurs hôtes. Plus précisément, dans le cas des poissons d'eau douce hôtes présentant une distribution disjonctive, ils reflètent à la fois des contacts historiques et contemporains. Le rôle des monogènes congénères spécifiques à leur hôte dans la révélation des contacts intercontinentaux et intracontinentaux historiques entre poissons d'eau douce est mis en évidence. Enfin, l'importance du rôle de la coadaptation génétique limitant la présence de monogènes spécifiques à l'hôte chez les poissons hybrides est soulignée.

Parasite abundance distribution as a model of host-parasite relationships between monogeneans Gyrodactylus spp. and cage-reared rainbow trout Oncorhynchus mykiss.

Aggregation is a fundamental feature of parasite distribution in the host population, but the biological implications of the aggregation indices used to describe the relationships between the populations of parasites and hosts are not evident. It is speculated that the form of distribution in each case is predicated on the host's varying resistance to the infection, which is hard to control, making it difficult to adequately interpret the index values. This paper examines several cases from trout farms in Russian Karelia to explore the monogenean Gyrodactylus spp. infection in rainbow trout of varying ages. The genetic homogeneity of cage-reared fish and the direct life cycle of the helminths make the relationship between the species more lucid than in natural host-parasite systems. The results give no ground to speak of any specific patterns: as well as in the natural systems, the infection rates in trout vary widely, i.e., the helminth distribution has not become more uniform; the observed distributions in all cases are adequately approximated by the negative binomial model; the positive abundance-occupancy relationships (AORs) and abundance-variance relationships (AVRs) common for parasitic systems apply to the basic infection parameters. The form of the negative binomial distribution is shaped by two parameters-k and θ, the former being a metric of the infection variability, which depends on the host's individual resistance, and the latter representing the parasites' reproduction and establishment success rates. A rise in the parameter k indicates increased aggregation and a higher parameter θ points to a more uniform frequency distribution. These parameters can be used as a representative tool for monitoring the parasite communities in salmonid fishes, including in aquaculture.

Symbiotic Algae of Acoel Species in the Seto Inland Sea and Symbiont Selectivity in the Hosts.

Praesagittifera naikaiensis is an acoel flatworm that inhabits the sandy beaches in the intertidal zone of the Seto Inland Sea. This species carries Tetraselmis sp., a green unicellular chlorophyte, as a symbiont in its body, and depends on algal photosynthetic products to survive. However, the eggs of P. naikaiensis contain no symbiotic algae, and juvenile P. naikaiensis acquire symbionts from the surrounding environment through horizontal transfer after hatching, thereby establishing new symbiotic relationships in each generation. Other acoel species, Symsagittifera spp., also inhabit the Seto Inland Sea shores and acquire symbiotic green algae via horizontal transfers. To characterize their symbionts, these acoels were collected from a wide area of the Seto Inland Sea and partial nucleotide sequences of the chloroplast ribulose diphosphate carboxylase large subunit (rbcL) of the symbiotic algae were determined and used for molecular phylogenetic analysis. Symbionts of both P. naikaiensis and Symsagittifera spp. belonged to the genus Tetraselmis but were phylogenetically distant, and both species established symbiotic relationships with different symbionts even when they were sympatric. To test whether each species selects specific algae in the environment for symbiosis, we established algal strains from P. naikaiensis and Symsagittifera sp. symbionts and conducted uptake experiments on aposymbiotic juveniles of P. naikaiensis. The results suggest that symbiotic algae from Symsagittifera could be taken up by P. naikaiensis juveniles, but were unable to establish a normal symbiotic relationship with the juveniles.

The Acoel nervous system: morphology and development.

Acoel flatworms have played a relevant role in classical (and current) discussions on the evolutionary origin of bilaterian animals. This is mostly derived from the apparent simplicity of their body architectures. This tenet has been challenged over the last couple of decades, mostly because detailed studies of their morphology and the introduction of multiple genomic technologies have unveiled a complexity of cell types, tissular arrangements and patterning mechanisms that were hidden below this 'superficial' simplicity. One tissue that has received a particular attention has been the nervous system (NS). The combination of ultrastructural and single cell methodologies has revealed unique cellular diversity and developmental trajectories for most of their neurons and associated sensory systems. Moreover, the great diversity in NS architectures shown by different acoels offers us with a unique group of animals where to study key aspects of neurogenesis and diversification od neural systems over evolutionary time.In this review we revisit some recent developments in the characterization of the acoel nervous system structure and the regulatory mechanisms that contribute to their embryological development. We end up by suggesting some promising avenues to better understand how this tissue is organized in its finest cellular details and how to achieve a deeper knowledge of the functional roles that genes and gene networks play in its construction.

Sperm competition favours intermediate sperm size in a hermaphrodite1.

Sperm competition is a potent mechanism of postcopulatory sexual selection that has been found to shape reproductive morphologies and behaviours in promiscuous animals. Especially sperm size has been argued to evolve in response to sperm competition through its effect on sperm longevity, sperm motility, the ability to displace competing sperm, and ultimately fertilization success. Additionally, sperm size has been observed to co-evolve with female reproductive morphology. Theoretical work predicts that sperm competition may select for longer sperm but may also favour shorter sperm if sperm size trades-off with number. In this study, we studied the relationship between sperm size and postmating success in the free-living flatworm, Macrostomum lignano. Specifically, we used inbred isolines of M. lignano that varied in sperm size to investigate how sperm size translated into the ability of worms to transfer and deposit sperm in a mating partner. Our results revealed a hump-shaped relationship with individuals producing sperm of intermediate size having the highest sperm competitiveness. This finding broadens our understanding of the evolution of sperm morphology by providing empirical support for stabilizing selection on sperm size under sperm competition.

The microbiome of the marine flatworm Macrostomum lignano provides fitness advantages and exhibits circadian rhythmicity.

The close association between animals and their associated microbiota is usually beneficial for both partners. Here, we used a simple marine model invertebrate, the flatworm Macrostomum lignano, to characterize the host-microbiota interaction in detail. This analysis revealed that the different developmental stages each harbor a specific microbiota. Studies with gnotobiotic animals clarified the physiological significance of the microbiota. While no fitness benefits were mediated by the microbiota when food was freely available, animals with microbiota showed significantly increased fitness with a reduced food supply. The microbiota of M. lignano shows circadian rhythmicity, affecting both the total bacterial load and the behavior of specific taxa. Moreover, the presence of the worm influences the composition of the bacterial consortia in the environment. In summary, the Macrostomum-microbiota system described here can serve as a general model for host-microbe interactions in marine invertebrates.

Geographic range, distribution patterns and interactions of Monogenea Van Beneden 1858, with species of native host freshwater fishes from Brazil / Distribuição geográfica, padrões de distribuição e interações de Monogenea Van Beneden 1858, com espécies de peixes hospedeiros nativos de água doce do Brasil

Abstract This paper investigated information on monogenean species using 312 scientific papers, to search for infection and geographic distribution patterns in native freshwater fish from Brazil. We used 1,698 samples of 296 fish species of 28 families distributed into Characiformes, Siluriformes, Cichliformes, Gymnotiformes, Perciformes, Mugiliformes, Osteoglossiformes and Clupeiformes, in addition to four hybrid fish. Among the hosts of the different orders and families, the greatest numbers of parasite-host associations were found for species of the families Serrasalmidae, Characidae, Loricariidae, Curimatidae and Anostomidae. The 578 species of monogeneans used in parasite-host interactions were distributed in 86 genera of six five families (Dactylogyridae, Gyrodactylidae, Diplectanidae, Microcotylidae, Ancylodiscoididae and Ancyrocephalidae), but with great predominance of Dactylogyridae species. There was variation in prevalence, intensity and abundance levels of monogeneans species among host fish species, as well as in infection sites that occurred predominantly in external organs. Positive correlations of prevalence, intensity and abundance with body length of hosts were observed. There was geographic distribution pattern of monogeneans limited mostly to two hydrographic basins those being the Amazon River and Paraná River. Just approximately 6% of potential monogeneans have been explored thus far, showing a clear need for further studies on this interesting group of parasites.

Resumo Este estudo investigou informações sobre espécies de monogenéticos, usando 312 artigos científicos para buscar padrões de infecção e distribuição geográfica em peixes nativos de água doce do Brasil. Foram utilizadas 1.698 amostras de 296 espécies de peixes de 28 famílias, distribuídas em Characiformes, Siluriformes, Cichliformes, Gymnotiformes, Perciformes, Mugiliformes, Osteoglossiformes e Clupeiformes, além de quatro peixes híbridos. Entre os hospedeiros das diferentes ordens e famílias, os maiores números de associações parasito-hospedeiro foram encontrados para espécies das famílias Serrasalmidae, Characidae, Loricariidae, Curimatidae e Anostomidae. As 578 espécies de monogenéticos, utilizadas nas interações parasito-hospedeiro, foram distribuídas em 86 gêneros de seis famílias (Dactylogyridae, Gyrodactylidae, Diplectanidae, Microcotylidae, Ancylodiscoididae e Ancyrocephalidae), mas com grande predominância de espécie de Dactylogyridae. Houve variação nos níveis de prevalência, intensidade e abundância das espécies de monogenéticos entre as espécies de peixes hospedeiros, bem como nos locais de infecção que ocorreram predominantemente em órgãos externos. Correlações positivas de prevalência, intensidade e abundância com o comprimento corporal dos hospedeiros foram observadas. Houve padrão de distribuição geográfica dos monogenéticos limitados principalmente a duas bacias hidrográficas, sendo elas o Rio Amazonas e Rio Paraná. Apenas aproximadamente 6% dos potenciais monogenéticos são conhecidos até agora, mostrando uma clara necessidade de mais estudos sobre esse interessante grupo de parasitos.

ON THAUMATOCOTYLE SCOTT, 1904 (MONOGENOIDEA: MONOCOTYLIDAE) AND THAUMATOCOTYLE PSEUDODASYBATIS HARGIS, 1955 WITH DESCRIPTIONS OF ITS PUTATIVE SIBLING SPECIES THAUMATOCOTYLE ADELPHA N. SP. AND THAUMATOCOTYLE CASIGNETA N. SP. PARASITIZING THE OLFACTORY ORGANS OF PELAGIC EAGLE RAYS (MYLIOBATIFORMES: AETOBATIDAE) IN THE PACIFIC OCEAN.

An emended diagnosis of ThaumatocotyleScott, 1904 (Monogenoidea: Monocotylidae) and a list of its species are provided. Merizocotyle urolophiChisholm and Whittington, 1999, Merizocotyle macrostrobusChisholm and Whittington, 2012, Merizocotyle papillaeChisholm and Whittington, 2012, and Merizocotyle rhadinopeosChisholm and Whittington, 2012 are transferred to Thaumatocotyle as new combinations. Thaumatocotyle pseudodasybatisHargis, 1955 is redescribed and is currently restricted to Thaumatocotyle-like helminths parasitizing the olfactory organs of the white-spotted eagle ray Aetobatus narinari (Euphrasen, 1790) (Myliobatiformes: Aetobatidae) in the western Atlantic Ocean. Two new species are described that infect the olfactory organs of pelagic eagle rays: Thaumatocotyle adelpha n. sp. from the ocellated eagle ray Aetobatus ocellatus (Kuhl, 1823) in the central and western Pacific Ocean and Thaumatocotyle casigneta n. sp. from the Pacific eagle ray Aetobatus laticeps Gill, 1865 from the eastern Pacific Ocean off the western coast of Mexico. Based on comparative morphology, T. pseudodasybatis, T. adelpha, and T. casigneta appear to form a subgroup of species that developed secondarily within the genus.

Embryonic development in the acoel Hofstenia miamia.

Acoels are marine worms that belong to the phylum Xenacoelomorpha, a deep-diverging bilaterian lineage. This makes acoels an attractive system for studying the evolution of major bilaterian traits. Thus far, acoel development has not been described in detail at the morphological and transcriptomic levels in a species in which functional genetic studies are possible. We present a set of developmental landmarks for embryogenesis in the highly regenerative acoel Hofstenia miamia. We generated a developmental staging atlas from zygote to hatched worm based on gross morphology, with accompanying bulk transcriptome data. Hofstenia embryos undergo a stereotyped cleavage program known as duet cleavage, which results in two large vegetal pole 'macromeres' and numerous small animal pole 'micromeres'. These macromeres become internalized as micromere progeny proliferate and move vegetally. We also noted a second, previously undescribed, cell-internalization event at the animal pole, following which we detected major body axes and tissues corresponding to all three germ layers. Our work on Hofstenia embryos provides a resource for mechanistic investigations of acoel development, which will yield insights into the evolution of bilaterian development and regeneration.

Molecular and morphological phylogeny of host-specific Dactylogyrus parasites (Monogenea) sheds new light on the puzzling Middle Eastern origin of European and African lineages.

BACKGROUND: Freshwater fauna of the Middle East encompass elements shared with three continents-Africa, Asia, and Europe-and the Middle East is, therefore, considered a historical geographic crossroad between these three regions. Even though various dispersion scenarios have been proposed to explain the current distribution of cyprinids in the peri-Mediterranean, all of them congruently suggest an Asian origin for this group. Herein, we investigated the proposed scenarios using monogenean parasites of the genus Dactylogyrus, which is host-specific to cyprinoid fishes. METHODS: A total of 48 Dactylogyrus species parasitizing cyprinids belonging to seven genera were used for molecular phylogenetic reconstruction. Taxonomically important morphological features, i.e., sclerotized elements of the attachment organ, were further evaluated to resolve ambiguous relationships between individual phylogenetic lineages. For 37 species, sequences of partial genes coding 18S and 28S rRNA, and the ITS1 region were retrieved from GenBank. Ten Dactylogyrus species collected from Middle Eastern cyprinoids and D. falciformis were de novo sequenced for the aforementioned molecular markers. RESULTS: The phylogenetic reconstruction divided all investigated Dactylogyrus species into four phylogenetic clades. The first one encompassed species with the "varicorhini" type of haptoral ventral bar with a putative origin linked to the historical dispersion of cyprinids via the North African coastline. The second clade included the majority of the investigated species parasitizing various phylogenetically divergent cyprinid hosts. The morphological and molecular data suggest the ancestral diversification of the species of this clade into two groups: (1) the group possessing the haptoral ventral bar of the "cornu" type, and (2) the group possessing the "wunderi" type. Dactylogyrus diversification apparently occurred in the Middle East, which is indicated by the presence of species with all morphotypes in the region. The last two clades included species parasitizing cyprinids with an East Asian origin, and species possessing the "magnihamatus" type of ventral bar. CONCLUSIONS: The molecular data suggest that some morphological characters of host-specific parasites may undergo convergent evolution in the divergent lineages, and therefore, to fully resolve the phylogenetic relationships among host-specific parasites, an integrative approach combining morphological and molecular data is still needed. In addition, our study indicates that parasite diversity in many regions is still under-explored, and thus we highlight the importance of studies of host-associated parasites, especially in the context of freshwater fish biogeography.