Dictyocoela microsporidia diversity and co-diversification with their host, a gammarid species complex (Crustacea, Amphipoda) with an old history of divergence and high endemic diversity

Abstract

Background Although the processes of co-evolution between parasites and their hosts are well known, evidence of co-speciation remains scarce. Microsporidian intracellular parasites, due to intimate relationships with their hosts and mixed mode of transmission (horizontal but also vertical, from mother to offspring), may represent an interesting biological model for investigating co-speciation. Amphipod crustaceans, especially gammarids, are regular hosts of microsporidian parasites, in particular the Dictyocoela spp., which have so far been found limited to these amphipods and are known to use a vertical mode of transmission. The amphipod genus Gammarus has a diversification history spanning the last 50–60 Mya and an extensive cryptic diversity in most of the nominal species. Here, we investigated the degree of co-diversification between Dictyocoela and Gammarus balcanicus, an amphipod with high degrees of ancient cryptic diversification and lineage endemism, by examining the genetic diversity of these parasites over the entire geographic range of the host. We hypothesised that the strong host diversification and vertical transmission of Dictyocoela would promote co-diversification. Results Using the parasite SSU rDNA as a molecular marker, analyzing 2225 host specimens from 88 sites covering whole host range, we found 31 haplogroups of Dictyocoela, 30 of which were novel, belonging to four Dictyocoela species already known to infect other Gammarus spp. The relationships between Dictyocoela and gammarids is therefore ancient, with the speciation in parasites preceding those of the hosts. Each novel haplogroup was nevertheless specific to G. balcanicus, leaving the possibility for subsequent co-diversification process during host diversification. A Procrustean Approach to Co-phylogeny (PACo) analysis revealed that diversification of Dictyocoela was not random with respect to that of the host. We found high degrees of congruence between the diversification of G. balcanicus and that of Dictyocoela roeselum and D. muelleri. However, we also found some incongruences between host and Dictyocoela phylogenies, e.g. in D. duebenum, probably due to host shifts between different G. balcanicus cryptic lineages. Conclusion The evolutionary history of Dictyocoela and Gammarus balcanicus represents an example of an overall host-parasite co-diversification, including cases of host shifts.

A new microsporidian parasite, Ordospora pajunii sp. nov (Ordosporidae), of Daphnia longispina highlights the value of genomic data for delineating species boundaries

“…colligata concomitantly with their respective crustacean hosts. Co‐speciation has been found in host‐parasite associations (Giraud et al, 2008), and microsporidia, being obligatory intracellular parasites that live in close proximity to their hosts, are prone to codiversification (Andreadis et al, 2012; Quiles et al, 2020). Indeed, different phylogeographic clades of O .…”

Wide geographic distribution of overlooked parasites: Rare Microsporidia in Gammarus balcanicus, a species complex with a high rate of endemism

“…Such a co-differentiation pattern has been suggested for Dictyocoela spp. from amphipods, both at large and local scales ( Park et al, 2020 ; Quiles et al, 2020 ). Exploring such a pattern further may benefit from the application of additional highly variable genetic markers in parasites, such as RPB1 (RNA polymerase II subunit 1), as already exemplified by Pretto et al (2018) , at least on microsporidian MOTUs where several haplogroups have now been detected in different gammarid species (e.g.…”

“…Samples used in the present study correspond to the G. balcanicus samples used by Mamos et al (2016) and Quiles et al (2020) . In short, G. balcanicus individuals were collected at 87 sites in 13 countries during several sampling campaigns between 2004 and 2016.…”

“…Gammarus balcanicus is in relative isolation from other European gammarids, since it rarely co-occurs with other gammarids ( Copilaș;-Ciocianu et al, 2014 ). During a survey of Microsporidia in the G. balcanicus complex over the entire host geographic range, we identified several lineages outside of the commonly identified N. granulosis and Dictyocoela taxa ( Quiles et al, 2020 ). These infections were considered ‘‘rare’’ (i.e.…”

Two parasites in one host: spatiotemporal dynamics and co-occurrence of Microsporidia and Rickettsia in an amphipod host

“…It is believed that Dictyocoela can be transmitted mainly vertically, horizontally, or both. However, which is the primary mode of transmission in each species is poorly understood (Quiles et al, 2020). Torix Rickettsia are known to be common in aquatic invertebrate hosts but their presence in amphipod hosts was only recently documented .…”