Abstract:Speciation via host-switching is a macroevolutionary process that emerges from a microevolutionary dynamic where individual parasites switch hosts, establish a new association, and reduce reproductive contact with the original parasite lineage. Phylogenetic distance and geographic distribution of the hosts have been shown to be determinants of the capacity and opportunity of the parasite to change hosts. Although speciation via host-switching has been reported in many host-parasite systems, its dynamic on the … Show more
“…Our results suggest that host switch plays a more important role in the coevolution process of gyrodactylids and their fish hosts than co-speciation and provides strong support to the previous finding that an adaptive mode of speciation associated with host switch is more prevalent than co-speciation among the gyrodactylids [ 18 ]. This finding also supports the proposal of a recent model study, which suggested that host switch can favor speciation in parasites [ 72 ]. Fig.…”
Background
Gyrodactylus is a lineage of monogenean flatworm ectoparasites exhibiting many features that make them a suitable model to study the host-parasite coevolutionary dynamics. Previous coevolutionary studies of this lineage mainly relied on low-power datasets (a small number of samples and a single molecular marker) and (now) outdated algorithms.
Methods
To investigate the coevolutionary relationship of gyrodactylids and their fish hosts in high resolution, we used complete mitogenomes (including two newly sequenced Gyrodactylus species), a large number of species in the single-gene dataset, and four different coevolutionary algorithms.
Results
The overall coevolutionary fit between the parasites and hosts was consistently significant. Multiple indicators confirmed that gyrodactylids are generally highly host-specific parasites, but several species could parasitize either multiple (more than 5) or phylogenetically distant fish hosts. The molecular dating results indicated that gyrodactylids tend to evolve towards high host specificity. Speciation by host switch was identified as a more important speciation mode than co-speciation. Assuming that the ancestral host belonged to Cypriniformes, we inferred four major host switch events to non-Cypriniformes hosts (mostly Salmoniformes), all of which occurred deep in the evolutionary history. Despite their relative rarity, these events had strong macroevolutionary consequences for gyrodactylid diversity. For example, in our dataset, 57.28% of all studied gyrodactylids parasitized only non-Cypriniformes hosts, which implies that the evolutionary history of more than half of all included lineages could be traced back to these major host switch events. The geographical co-occurrence of fishes and gyrodactylids determined the host use by these gyrodactylids, and geography accounted for most of the phylogenetic signal in host use.
Conclusions
Our findings suggest that the coevolution of Gyrodactylus flatworms and their hosts is largely driven by geography, phylogeny, and host switches.
Graphical Abstract
“…Our results suggest that host switch plays a more important role in the coevolution process of gyrodactylids and their fish hosts than co-speciation and provides strong support to the previous finding that an adaptive mode of speciation associated with host switch is more prevalent than co-speciation among the gyrodactylids [ 18 ]. This finding also supports the proposal of a recent model study, which suggested that host switch can favor speciation in parasites [ 72 ]. Fig.…”
Background
Gyrodactylus is a lineage of monogenean flatworm ectoparasites exhibiting many features that make them a suitable model to study the host-parasite coevolutionary dynamics. Previous coevolutionary studies of this lineage mainly relied on low-power datasets (a small number of samples and a single molecular marker) and (now) outdated algorithms.
Methods
To investigate the coevolutionary relationship of gyrodactylids and their fish hosts in high resolution, we used complete mitogenomes (including two newly sequenced Gyrodactylus species), a large number of species in the single-gene dataset, and four different coevolutionary algorithms.
Results
The overall coevolutionary fit between the parasites and hosts was consistently significant. Multiple indicators confirmed that gyrodactylids are generally highly host-specific parasites, but several species could parasitize either multiple (more than 5) or phylogenetically distant fish hosts. The molecular dating results indicated that gyrodactylids tend to evolve towards high host specificity. Speciation by host switch was identified as a more important speciation mode than co-speciation. Assuming that the ancestral host belonged to Cypriniformes, we inferred four major host switch events to non-Cypriniformes hosts (mostly Salmoniformes), all of which occurred deep in the evolutionary history. Despite their relative rarity, these events had strong macroevolutionary consequences for gyrodactylid diversity. For example, in our dataset, 57.28% of all studied gyrodactylids parasitized only non-Cypriniformes hosts, which implies that the evolutionary history of more than half of all included lineages could be traced back to these major host switch events. The geographical co-occurrence of fishes and gyrodactylids determined the host use by these gyrodactylids, and geography accounted for most of the phylogenetic signal in host use.
Conclusions
Our findings suggest that the coevolution of Gyrodactylus flatworms and their hosts is largely driven by geography, phylogeny, and host switches.
Graphical Abstract
“…(i) The parasite has to establish new associations with the host after transition, and an array of behavioral, physiological, and phenological adaptations are prerequisites to successful adaptations. The hosts' phylogenetic distance determines the parasite's capacity and opportunity to change hosts (D'Bastiani et al, 2023). In our case, each host species, regardless of ground-living or arboricolous, belong to a not very deeply diverging monophyletic lineage called T. unifasciatus group (Prebus, 2017) that may not differ substantially from each other in their life cycle characteristics.…”
Section: Discussionmentioning
confidence: 91%
“…Differential selection and adaptation to different abiotic and biotic environmental factors are often believed to be one of the primary drivers of speciation (Maron et al, 2019;Nosil, 2012). One of the most specific environmental transitions, hostswitching in parasites, has been reported to foster speciation in many host-parasite systems, ascribed to reproductive isolation after establishing a new association with the novel host species (D'Bastiani et al, 2023) and the fact that specific environmental differences may affect genetic traits that trigger speciation processes (Cini et al, 2015;Schluter, 2001). This phenomenon is believed to boost diversity in many specialist herbivores, like gall-inducing plant parasites (Jones et al, 2022;Tilmon & Tilmon, 2008), and parasites (Johnson et al, 2016;Martins et al, 2021), including social parasites (Buschinger, 2009;Lenoir et al, 2001;Savolainen & Deslippe, 1996).…”
Host–parasite systems, including social parasites that exploit resources of the host colonies, are fascinating objects for evolutionary biologists mainly due to the dynamic and often rapid host–parasite coevolution. Host‐switching events are believed to induce rapid speciation of parasitic species. The socially parasitic ant lineage Myrmoxenus, which corresponds to the monophyletic Temnothorax corsicus group, counts in total a dozen species. Most Myrmoxenus species utilize a single host species, but a few others, like Myrmoxenus ravouxi (André, 1896) and M. gordiagini Ruzsky, 1902, are known to use multiple host taxa. Myrmoxenus zaleskyi (Sadil, 1953) was described as a putative congener of M. ravouxi based on its distinct host selection. In this paper, we investigate the diversity of the widely distributed European lineages M. ravouxi and M. zaleskyi from multiple and complementary perspectives to understand whether the host preference exhibited by these two forms implies speciation. We integrated evidence from molecular genetics using mitochondrial CO I/CO II genes, including the tLeu‐region, and multivariate analyses of morphometric data collected from workers and female sexuals (gynes). Although there is substantial regional host species specificity, results suggest that host switching did not result in phylogenetic or morphological divergence and that the central European M. zaleskyi can be considered the junior synonym of M. ravouxi. As the lineage Myrmoxenus has been the subject of considerable evolutionary research, these results are essential to achieve a more accurate picture of host–parasite systems in the future and further strengthen the justification of an integrative approach in studying similarly complex systems. We advise against describing new parasitic species based on host preference unless coupled with marked heritable phenotypic adaptations.
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