Linking bacterial communities associated with the environment and the ecosystem engineer <i>Orchestia gammarellus</i> at contrasting salt marsh elevations

The digestive tract of animals harbors microbiota important for the host’s fitness and performance. The interaction between digestive tract bacteria and soil animal hosts is still poorly explored despite the importance of soil fauna for ecosystem processes. In this study, we investigated the interactions between the bacterial communities from the digestive tract of the litter-feeding, semi-terrestrial crustacean Orchestia gammarellus and those obtained from the environment; these organisms thrive in, i.e., soil and plant litter from salt marshes. We hypothesized that elevation is an important driver of soil and litter bacterial communities, which indirectly (via ingested soil and litter bacteria) influences the bacterial communities in the digestive tract of O. gammarellus. Indeed, our results revealed that elevation modulated soil and litter bacterial community composition along with soil organic matter content and the C:N ratio. Soil and plant litter differed in alpha diversity indexes (richness and diversity), and in the case of plant litter, both indexes increased with elevation. In contrast, elevation did not affect the composition of bacterial communities associated with O. gammarellus’ digestive tract, suggesting selection by the host, despite the fact that a large component of the bacterial community was also detected in external sources. Importantly, Ca. Bacilloplasma and Vibrio were highly prevalent and abundant in the host. The taxonomic comparison of Ca. Bacilloplasma amplicon sequence variants across the host at different elevations suggested a phylogenetic divergence due to host habitat (i.e., marine or semi-terrestrial), thus supporting their potential functional role in the animal physiology. Our study sheds light on the influence of the environment on soil animal–bacteria interactions and provides insights into the resilience of the O. gammarellus–associated bacteria to increased flooding frequency

Sex ratios of the tick Ixodes arboricola are strongly female-biased, but there are no indications of sex-distorting bacteria

International audienceStudies on sex ratio are of fundamental importance for understanding the biology of populations and biological control of pests and pathogens. In most Ixodes tick species, only females feed in the adult stage and, hence, contribute to pathogen transmission. The tree-hole tick Ixodes arboricola infests cavity-nesting birds and has limited dispersal possibilities. It plays an important role in the maintenance of zoonotic disease cycles. Here, we quantified the sex ratio of 718 adult I. arboricola ticks obtained from a laboratory stock at nine distinct periods (cohorts) from 2008 to 2015. In addition, we screened 93 specimens, collected from four study sites in 2011 and 2012, for the presence of six maternally inherited bacterial parasites known to manipulate arthropod sex ratios. We found significantly female-biased sex ratios in seven out of nine cohorts. There were no infections with members of the Wolbachia, Arsenophonus or Cardinium bacterial genera, whereas 96.8% of the screened ticks were infected with Rickettsia vini, 22.6% with Rickettsiella sp., and 14.0% with Spiroplasma ixodetis. Male and female I. arboricola were found equally infected. Our results suggest skewed sex ratios in I. arboricola are not caused by these bacterial infections, although there may be other, untested candidates driving sex ratios. Alternatively, female-biased sex ratios may be an adaptation in females to high local densities and low dispersal, where the production of daughters has a selective advantage because a few sons can fertilise all daughters

An experimental test to compare potential and realised specificity in ticks with different ecologies

The majority of studies on ecological specialisation rely on data reflecting realised specificity, without considering species’ potential specificity. Most species of ticks, a large family of hematophagous ectoparasites, have a narrow host range in nature, but it is unclear whether this is due to host-driven adaptations or other processes (such as off-host abiotic environment). We investigated the potential specificity of two tick species with contrasting ecology by infesting three avian host species that occur in the same off-host macrohabitat but are unequally infested by the ticks in nature (i.e. have contrasting realised specificity). The endophilic specialist tick Ixodes arboricola resides inside the hosts’ nest and has high realised host specificity, whereas the exophilic generalist tick I. ricinus encounters hosts in the field and has very low realised specificity. As hosts, we used great tits (frequently infested by both tick species), blackbirds (frequently infested by I. ricinus but never by I. arboricola) and great spotted woodpeckers (no ticks of either species have been reported). If realised specificity is constrained by host-driven adaptations there should be no differences between potential and realised specificity, whereas if realised specificity is constrained by other processes potential specificity and realised specificity should be different. We found that attachment rates and weight during feeding of I. arboricola were lower on blackbirds than on great tits, whereas there were no such differences for I. ricinus. No ticks of either species attached to woodpeckers. These results indicate that realised host specificity of ticks is, at least partially, constrained by host-driven adaptations. This specificity therefore strongly depends on the ticks’ encounter rates with particular host types, which are affected by the ticks’ off-host ecological requirements, behaviour and life-history characteristics

SPAGeDi file

Alleles from seven microsatellite loci in SPAGeDi format of ticks collected from nest boxes in woodlots near Antwerp, Belgium. Coordinates are used to indicate instar

Arlequin file

Alleles from seven microsatellite loci in Arlequin format of ticks collected from nest boxes in woodlots near Antwerp, Belgium. Ticks are grouped per nest box, and structured per woodlot

Pairwise distance matrix

Pairwise distance matrix between all nest boxes. Distances are absolute differences between geographical position (degrees lattitude and longitude)

GenePop file

Alleles from seven microsatellite loci in GenePop format of ticks collected from nest boxes in woodlots near Antwerp, Belgiu

Evolutionary changes in symbiont community structure in ticks

International audienceEcological specialization to restricted diet niches is driven by obligate, and often maternally inherited, symbionts in many arthropod lineages. These heritable symbionts typically form evolutionarily stable associations with arthropods that can last for millions of years. Ticks were recently found to harbour such an obligate symbiont, Coxiella-LE, that synthesizes B vitamins and cofactors not obtained in sufficient quantities from blood diet. In this study, the examination of 81 tick species shows that some Coxiella-LE symbioses are evolutionarily stable with an ancient acquisition followed by codiversification as observed in ticks belonging to the Rhipicephalus genus. However, many other Coxiella-LE symbioses are characterized by low evolutionary stability with frequent host shifts and extinction events. Further examination revealed the presence of nine other genera of maternally inherited bacteria in ticks. Although these nine symbionts were primarily thought to be facultative, their distribution among tick species rather suggests that at least four may have independently replaced Coxiella-LE and likely represent alternative obligate symbionts. Phylogenetic evidence otherwise indicates that cocladogenesis is globally rare in these symbioses as most originate via horizontal transfer of an existing symbiont between unrelated tick species. As a result, the structure of these symbiont communities is not fixed and stable across the tick phylogeny. Most importantly, the symbiont communities commonly reach high levels of diversity with up to six unrelated maternally inherited bacteria coexisting within host species. We further conjecture that interactions among coexisting symbionts are pivotal drivers of community structure both among and within tick species

An experimental test to compare potential and realised specificity in ticks with different ecologies

The majority of studies on ecological specialisation rely on data reflecting realised specificity, without considering species’ potential specificity. Most species of ticks, a large family of hematophagous ectoparasites, have a narrow host range in nature, but it is unclear whether this is due to host-driven adaptations or other processes (such as off-host abiotic environment). We investigated the potential specificity of two tick species with contrasting ecology by infesting three avian host species that occur in the same off-host macrohabitat but are unequally infested by the ticks in nature (i.e. have contrasting realised specificity). The endophilic specialist tick Ixodes arboricola resides inside the hosts’ nest and has high realised host specificity, whereas the exophilic generalist tick I. ricinus encounters hosts in the field and has very low realised specificity. As hosts, we used great tits (frequently infested by both tick species), blackbirds (frequently infested by I. ricinus but never by I. arboricola) and great spotted woodpeckers (no ticks of either species have been reported). If realised specificity is constrained by host-driven adaptations there should be no differences between potential and realised specificity, whereas if realised specificity is constrained by other processes potential specificity and realised specificity should be different. We found that attachment rates and weight during feeding of I. arboricola were lower on blackbirds than on great tits, whereas there were no such differences for I. ricinus. No ticks of either species attached to woodpeckers. These results indicate that realised host specificity of ticks is, at least partially, constrained by host-driven adaptations. This specificity therefore strongly depends on the ticks’ encounter rates with particular host types, which are affected by the ticks’ off-host ecological requirements, behaviour and life-history characteristics