Gut microbial ecology of lizards: insights into diversity in the wild,effects of captivity,variation across gut regions and transmission

Animals maintain complex associations with a diverse microbiota living in their guts. Our understanding of the ecology of these associations is extremely limited in reptiles. Here, we report an in‐depth study into the microbial ecology of gut communities in three syntopic and viviparous lizard species (two omnivores: Liolaemus parvus and Liolaemus ruibali and an herbivore: Phymaturus williamsi). Using 16S rRNA gene sequencing to inventory various bacterial communities, we elucidate four major findings: (i) closely related lizard species harbour distinct gut bacterial microbiota that remain distinguishable in captivity; a considerable portion of gut bacterial diversity (39.1%) in nature overlap with that found on plant material, (ii) captivity changes bacterial community composition, although host‐specific communities are retained, (iii) faecal samples are largely representative of the hindgut bacterial community and thus represent acceptable sources for nondestructive sampling, and (iv) lizards born in captivity and separated from their mothers within 24 h shared 34.3% of their gut bacterial diversity with their mothers, suggestive of maternal or environmental transmission. Each of these findings represents the first time such a topic has been investigated in lizard hosts. Taken together, our findings provide a foundation for comparative analyses of the faecal and gastrointestinal microbiota of reptile hosts.     

Effectively vertical transmission of a Drosophila‐parasitic nematode: mechanism and consequences

1. Long‐term control of insects by parasites is possible only if the parasite populations persist. Because parasite transmission rate depends on host density, parasite populations may go extinct during periods of low host density. Vertical transmission of parasites, however, is independent of host density and may therefore provide a demographic bridge through times when their insect hosts are rare. 2. The nematode Howardula aoronymphium, which parasitises mycophagous species of Drosophila, can experience both horizontal and effectively vertical transmission, relative rates of which depend, in theory at least, on the density of hosts at breeding sites. 3. A nine‐generation experiment was carried out in which nematodes were transmitted either exclusively vertically or primarily horizontally. This experiment revealed that these parasites can persist and exhibit positive population growth even when there is only vertical transmission. 4. Assays at the end of the experiment revealed that the vertically transmitted nematodes had suffered no inbreeding depression and that they were similar to the horizontally transmitted nematodes in terms of virulence, infectivity, within‐host growth rate, and fecundity. Thus, vertical transmission of H. aoronymphium did not appear to compromise the ability of these parasites to control Drosophila populations.     

Genotypic and phenotypic variation in transmission traits of a complex life cycle parasite

Characterizing genetic variation in parasite transmission traits and its contribution to parasite vigor is essential for understanding the evolution of parasite life‐history traits. We measured genetic variation in output, activity, survival, and infection success of clonal transmission stages (cercaria larvae) of a complex life cycle parasite (Diplostomum pseudospathaceum). We further tested if variation in host nutritional stage had an effect on these traits by keeping hosts on limited or ad libitum diet. The traits we measured were highly variable among parasite genotypes indicating significant genetic variation in these life‐history traits. Traits were also phenotypically variable, for example, there was significant variation in the measured traits over time within each genotype. However, host nutritional stage had no effect on the parasite traits suggesting that a short‐term reduction in host resources was not limiting the cercarial output or performance. Overall, these results suggest significant interclonal and phenotypic variation in parasite transmission traits that are not affected by host nutritional status.     

Global patterns in helminth host specificity: phylogenetic and functional diversity of regional host species pools matter

Host specificity has a major influence on a parasite's ability to shift between human and animal host species. Yet there is a dearth of quantitative approaches to explore variation in host specificity across biogeographical scales, particularly in response to the varying community compositions of potential hosts. We built a global dataset of intermediate host associations for nine of the world's most widespread helminth parasites (all of which infect humans). Using hierarchical models, we asked if realised parasite host specificity varied in response to regional variation in the phylogenetic and functional diversities of potential host species. Parasites were recorded in 4–10 zoogeographical regions, with some showing considerable geographical variation in observed versus expected host specificity. Parasites generally exhibited the lowest phylogenetic host specificity in regions with the greatest variation in prospective host phylogenetic diversity, namely the Neotropical, Saharo‐Arabian and Australian regions. Globally, we uncovered notable variation in parasite host shifting potential. Observed host assemblages for Hydatigera taeniaeformis and Hymenolepis diminuta were less phylogenetically diverse than expected, suggesting limited potential to spillover into unrelated hosts. Host assemblages for Echinococcus granulosus, Mesocestoides lineatus and Trichinella spiralis were less functionally diverse than expected, suggesting limited potential to shift across host ecological niches. By contrast, Hyd. taeniaeformis infected a higher functional diversity of hosts than expected, indicating strong potential to shift across hosts with different ecological niches. We show that the realised phylogenetic and functional diversities of infected hosts are determined by biogeographical gradients in prospective host species pools. These findings emphasise the need to account for underlying species diversity when assessing parasite host specificity. Our framework to identify variation in realised host specificity is broadly applicable to other host–parasite systems and will provide key insights into parasite invasion potential at regional and global scales.     

Symbiont‐conferred protection against Hymenopteran parasitoids in aphids: how general is it?

1. Hosts are often targeted by multiple species of parasites, leading to a confluence of selective pressures on them. In response, hosts may either evolve defences that act very generally, or specific defences against particular parasites. Aphids are attacked by multiple species of endoparasitoid wasps, and there is clear evidence that heritable endosymbionts can confer resistance against some of these wasps. Less clear is how symbiont‐conferred resistance in a single host acts against multiple parasitoid species. 2. This question was addressed in the black bean aphid, Aphis fabae (Scopoli). Unprotected aphids and aphids protected by three different strains of the defensive endosymbiont Hamiltonella defensa were exposed to four species of parasitic wasps: the parthenogenetic species Lysiphlebus fabarum (Marshall), which was represented by three different asexual lines, and the sexual species Aphidius colemani (Viereck), Binodoxys angelicae (Halliday), and Aphelinus chaonia (Walker). 3. Hamiltonella defensa provided strong protection against L. fabarum and Aphidius colemani, but there was no evidence that H. defensa‐infected aphids were more resistant to the other parasitoid species. While Aphidius colemani was virtually unable to parasitise any aphids harbouring H. defensa, there was variation among the three asexual lines of L. fabarum in how susceptible they were to the defence provided by the different symbiont strains, resulting in a significant genotype‐by‐genotype interaction. 4. The present results suggest that symbiosis with H. defensa does not provide aphids with a general defence against parasitoid wasps, possibly because some species have evolved specific counter adaptations or because biological differences preclude the symbiont's effectiveness against these species.     

Parasite predators exhibit a rapid numerical response to increased parasite abundance and reduce transmission to hosts

Predators of parasites have recently gained attention as important parts of food webs and ecosystems. In aquatic systems, many taxa consume free‐living stages of parasites, and can thus reduce parasite transmission to hosts. However, the importance of the functional and numerical responses of parasite predators to disease dynamics is not well understood. We collected host–parasite–predator cooccurrence data from the field, and then experimentally manipulated predator abundance, parasite abundance, and the presence of alternative prey to determine the consequences for parasite transmission. The parasite predator of interest was a ubiquitous symbiotic oligochaete of mollusks, Chaetogaster limnaei limnaei, which inhabits host shells and consumes larval trematode parasites. Predators exhibited a rapid numerical response, where predator populations increased or decreased by as much as 60% in just 5 days, depending on the parasite:predator ratio. Furthermore, snail infection decreased substantially with increasing parasite predator densities, where the highest predator densities reduced infection by up to 89%. Predators of parasites can play an important role in regulating parasite transmission, even when infection risk is high, and especially when predators can rapidly respond numerically to resource pulses. We suggest that these types of interactions might have cascading effects on entire disease systems, and emphasize the importance of considering disease dynamics at the community level.     

Haemoplasmas in wild rodents: Routes of transmission and infection dynamics

The way that some parasites and pathogens persist in the hostile environment of their host for long periods remains to be resolved. Here, longitudinal field surveys were combined with laboratory experiments to investigate the routes of transmission and infection dynamics of such a pathogen—a wild rodent haemotropic bacterium, specifically a Mycoplasma haemomuris‐like bacterium. Fleaborne transmission, direct rodent‐to‐rodent transmission and vertical transmission from fleas or rodents to their offspring were experimentally quantified, and indications were found that the main route of bacterial transmission is direct, although its rate of successful transmission is low (~20%). The bacterium's temporal dynamics was then compared in the field to that observed under a controlled infection experiment in field‐infected and laboratory‐infected rodents, and indications were found, under all conditions, that the bacterium reached its peak infection level after 25–45 days and then decreased to low bacterial loads, which persist for the rodent's lifetime. These findings suggest that the bacterium relies on persistency with low bacterial loads for long‐term coexistence with its rodent host, having both conceptual and applied implications.     

Host traits associated with species roles in parasite sharing networks

The community of host species that a parasite infects is often explained by functional traits and phylogeny, predicting that closely related hosts or those with particular traits share more parasites with other hosts. Previous research has examined parasite community similarity by regressing pairwise parasite community dissimilarity between two host species against host phylogenetic distance. However, pairwise approaches cannot target specific host species responsible for disproportionate levels of parasite sharing. To better identify why some host species contribute differentially to parasite diversity patterns, we represent parasite sharing using ecological networks consisting of host species connected by instances of shared parasitism. These networks can help identify host species and traits associated with high levels of parasite sharing that may subsequently identify important hosts for parasite maintenance and transmission within communities. We used global‐scale parasite sharing networks of ungulates, carnivores, and primates to determine if host importance – encapsulated by the network measures degree, closeness, betweenness, and eigenvector centrality – was predictable based on host traits. Our findings suggest that host centrality in parasite sharing networks is a function of host population density and range size, with range size reflecting both species geographic range and the home range of those species. In the full network, host taxonomic family became an important predictor of centrality, suggesting a role for evolutionary relationships between host and parasite species. More broadly, these findings show that trait data predict key properties of ecological networks, thus highlighting a role for species traits in understanding network assembly, stability, and structure.     

A tale of two lineages: unexpected,long‐term persistence of the amphibian‐killing fungus in Brazil

For the past 17 years, scientists have been compiling a list of amphibian species susceptible to infection by the amphibian‐killing chytrid fungus, Batrachochytrium dendrobatidis (Bd), all over the world, with >500 species infected on every continent except Antarctica (Olson et al. 2013 ). Where Bd has been found, the impacts on amphibians has been one of two types: either Bd arrives into a naïve amphibian population followed by a mass die‐off and population declines (e.g. Lips et al. 2006 ), or Bd is present at some moderate prevalence, usually infecting many species but at apparently nonlethal intensities for a long time. In this issue of Molecular Ecology, Rodriguez et al. ( 2014 ) discover that the Atlantic Coastal Forest of Brazil is home to two Bd lineages: the Global Pandemic Lineage (Bd‐GPL) – the strain responsible for mass die‐offs and population declines – and a lineage endemic to Brazil (Bd‐Bz). Even more surprising was that both lineages have been present in this area for the past 100 years, making these the oldest records of Bd infecting amphibians. The team also described a moderate but steady prevalence of ~20% across all sampled anuran families for over 100 years, indicating that Brazil has been in an enzootic disease state for over a century. Most amphibians were infected with Bd‐GPL, suggesting this lineage may be a better competitor than Bd‐Bz or may be replacing the Bd‐Bz lineage. Rodriguez et al. ( 2014 ) also detected likely hybridization of the two Bd lineages, as originally described by Schloegel et al. ( 2012 ).     

Natural selection on quantitative immune defence traits: a comparison between theory and data

Parasites present a threat for free‐living species and affect several ecological and evolutionary processes. Immune defence is the main physiological barrier against infections, and understanding its evolution is central for predicting disease dynamics. I review theoretical predictions and empirical data on natural selection on quantitative immune defence traits in the wild. Evolutionary theory predicts immune traits to be under stabilizing selection owing to trade‐offs between immune function and life‐history traits. Empirical data, however, support mainly positive directional selection, but also show variation in the form of selection among study systems, immune traits and fitness components. I argue that the differences between theory and empirical data may at least partly arise from methodological difficulties in testing stabilizing selection as well as measuring fitness. I also argue that the commonness of positive directional selection and the variation in selection may be caused by several biological factors. First, selection on immune function may show spatial and temporal variation as epidemics are often local/seasonal. Second, factors affecting the range of phenotypic variation in immune traits could alter potential for selection. Third, different parasites may impose different selective pressures depending on their characteristics. Fourth, condition dependence of immune defence can obscure trade‐offs related to it, thus possibly modifying observed selection gradients. Fifth, nonimmunological defences could affect the form of selection by reducing the benefits of strong immune function. To comprehensively understand the evolution of immune defence, the role of above factors should be considered in future studies.     

Feather mites play a role in cleaning host feathers: New insights from DNA metabarcoding and microscopy

Parasites and other symbionts are crucial components of ecosystems, regulating host populations and supporting food webs. However, most symbiont systems, especially those involving commensals and mutualists, are relatively poorly understood. In this study, we have investigated the nature of the symbiotic relationship between birds and their most abundant and diverse ectosymbionts: the vane‐dwelling feather mites. For this purpose, we studied the diet of feather mites using two complementary methods. First, we used light microscopy to examine the gut contents of 1,300 individual feather mites representing 100 mite genera (18 families) from 190 bird species belonging to 72 families and 19 orders. Second, we used high‐throughput sequencing (HTS) and DNA metabarcoding to determine gut contents from 1,833 individual mites of 18 species inhabiting 18 bird species. Results showed fungi and potentially bacteria as the main food resources for feather mites (apart from potential bird uropygial gland oil). Diatoms and plant matter appeared as rare food resources for feather mites. Importantly, we did not find any evidence of feather mites feeding upon bird resources (e.g., blood, skin) other than potentially uropygial gland oil. In addition, we found a high prevalence of both keratinophilic and pathogenic fungal taxa in the feather mite species examined. Altogether, our results shed light on the long‐standing question of the nature of the relationship between birds and their vane‐dwelling feather mites, supporting previous evidence for a commensalistic–mutualistic role of feather mites, which are revealed as likely fungivore–microbivore–detritivore symbionts of bird feathers.     

Mistletoe macroecology: spatial patterns in species diversity and host use across Australia

Mistletoes are parasitic plants, the spatial distributions of which are poorly understood on macroecological scales. Because of their highly unusual life history, investigating mistletoe macroecology may provide new insight into broad‐scale patterns in species distributions. We collated data on the spatial distribution and host use of 65 species of Loranthaceous mistletoes across the continent of Australia, and tested two predictions. First, we predicted mistletoe diversity would be unrelated to productivity (i.e. evapotranspiration and precipitation), as the parasitic lifestyle might relax environmental constraints on their distributions. Second, we predicted that mistletoe host ranges (number of infected host species) would increase in areas with more potential host species. The basis of this prediction is that greater host generality is likely to evolve in regions with greater host diversity because of greater unpredictability in encounter rates with particular host species. Conversely, in regions with fewer potential hosts, randomly dispersing mistletoe propagules are likely to repeatedly encounter particular host species, thus favouring the evolution of host specialization. The results were generally consistent with these predictions. Mistletoe diversity across Australia was weakly associated with environmental conditions, whereas mistletoe host ranges increased significantly with total plant diversity. Macroecological patterns in mistletoes are unusual. In contrast to non‐parasitic plants, mistletoe diversity is poorly correlated with productivity. Host ranges varied predictably across Australia, providing the first quantitative support for the hypothesis that mistletoes in diverse regions tend to be host generalists, whereas mistletoes in depauperate regions tend to be host specialists. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 459–468.     

Mechanisms structuring host–parasitoid networks in a global warming context: a review

1. In natural communities, multiple host and parasitoid species are linked to form complex networks of trophic and non‐trophic interactions. Understanding how these networks will respond to global warming is of wide relevance for agriculture and conservation. 2. This study synthesises the emerging evidence surrounding host–parasitoid networks in the context of global warming. The suite of direct and indirect interaction types within host–parasitoid networks is summarised, as well as their sensitivity to temperature changes. The study also compiles and reviews studies investigating the responses of whole host–parasitoid networks to increasing temperatures or proxy variables. The findings reveal there is limited evidence overall for the prediction that parasitism will be reduced under global warming: approximately equal numbers of studies show elevated and reduced parasitism. 3. Increasingly, endosymbiotic bacteria are recognised as influential mediators of host–parasitoid interactions. These endosymbionts can change how individual species respond to global warming, and their effects can cascade to affect whole host–parasitoid networks. The evidence that symbiotic bacteria are likely to affect the response of host–parasitoid networks to global warming is reviewed. Symbionts can protect hosts from their parasitoids or influence thermal tolerance of their host species. Furthermore, the symbionts themselves can be impacted by global warming. 4. Finally, the study considers the most promising avenues for future research into the mechanisms structuring host–parasitoid networks in the context of global warming. Alongside the increasing availability of modern molecular methods to document the structure of real, species‐rich host–parasitoid networks, the study highlights the utility of manipulative experiments and mathematical models.     

Effects of nematode parasitism on mycophagous drosophilid species in northern Japan

Mycophagous drosophilids and their nematode parasites were studied in an intensive census conducted throughout the active season over four years (2000–2003) in Hokkaido, northern Japan. Using census data, I assessed the prevalence of nematode parasitism through seasons, determined its effects on drosophilid female fertility and tested the “disproportionate parasitism hypothesis” to evaluate its effects on drosophilid community structure. Over the four‐year census, a total of 43 fungal species were found on the census route and 18 177 adult drosophilid flies were collected. The yearly parasitism rate on the total drosophilid community varied from 6.2% in 2000 to 5.1% in 2001 and 3.0% in 2002 and 2003. There was strong seasonal variation in the prevalence of parasitism. In addition, parasitism rates varied among drosophilid species. All parasitized females carried only small numbers of eggs. Thus, nematode parasitism had a strong deleterious effect on the fitness of infected flies. The relative abundance of drosophilid species and parasitism rate were not significantly correlated. Thus, the disproportionate parasitism hypothesis likely does not apply to the mycophagous drosophilid community in Japan.     

Virulence‐driven trade‐offs in disease transmission: A meta‐analysis*

The virulence–transmission trade‐off hypothesis proposed more than 30 years ago is the cornerstone in the study of host–parasite co‐evolution. This hypothesis rests on the premise that virulence is an unavoidable and increasing cost because the parasite uses host resources to replicate. This cost associated with replication ultimately results in a deceleration in transmission rate because increasing within‐host replication increases host mortality. Empirical tests of predictions of the hypothesis have found mixed support, which cast doubt about its overall generalizability. To quantitatively address this issue, we conducted a meta‐analysis of 29 empirical studies, after reviewing over 6000 published papers, addressing the four core relationships between (1) virulence and recovery rate, (2) within‐host replication rate and virulence, (3) within‐host replication and transmission rate, and (4) virulence and transmission rate. We found strong support for an increasing relationship between replication and virulence, and replication and transmission. Yet, it is still uncertain if these relationships generally decelerate due to high within‐study variability. There was insufficient data to quantitatively test the other two core relationships predicted by the theory. Overall, the results suggest that the current empirical evidence provides partial support for the trade‐off hypothesis, but more work remains to be done.     

Disappearance of eggs from nonparasitized nests of brood parasite hosts: the evolutionary equilibrium hypothesis revisited

The evolutionary equilibrium hypothesis was proposed to explain variation in egg rejection rates among individual hosts (intra‐ and interspecific) of avian brood parasites. Hosts may sometimes mistakenly reject own eggs when they are not parasitized (i.e. make recognition errors). Such errors would incur fitness costs and could counter the evolution of host defences driven by costs of parasitism (i.e. creating equilibrium between acceptors and rejecters within particular host populations). In the present study, we report the disappearance of host eggs from nonparasitized nests in populations of seven actual and potential hosts of the common cuckoo Cuculus canorus. Based on these data, we calculate the magnitude of the balancing parasitism rate provided that all eggs lost are a result of recognition errors. Importantly, because eggs are known to disappear from nests for reasons other than erroneous host rejection, our data represent the maximum estimates of such costs. Nonetheless, the disappearance of eggs was a rare event and therefore incurred low costs compared to the high costs of parasitism. Hence, costs as a result of recognition errors are probably of minor importance with respect to opposing selective pressure for the evolution of egg rejection in these hosts. We cannot exclude the possibility that low or intermediate egg rejection rates in some host populations may be caused by spatiotemporal variation in the occurrence of parasitism and gene flow, creating a variable influence of opposing costs as a result of recognition errors and the costs of parasitism.     

Priming of host resistance to protect cultured rainbow trout Oncorhynchus mykiss against eye flukes and parasite‐induced cataracts

In the present study, immunologically naive rainbow trout Oncorhynchus mykiss were experimentally exposed to a low‐level Diplostomum spathaceum (Trematoda) infection to stimulate acquired resistance and, along with unexposed controls, were subsequently exposed to natural infection for 8 weeks. The priming of the host resistance, designed to simulate a procedure applicable in aquaculture, decreased the number of establishing parasites compared to untreated controls by the end of the experiment. This effect was slow and did not protect the fish against the parasite‐induced cataracts. The results suggest that this type of priming of host resistance is probably inefficient in preventing the deleterious effects of D. spathaceum infection in aquaculture conditions.     

Cophylogenetic assessment of New World warblers (Parulidae) and their symbiotic feather mites (Proctophyllodidae)

Host–symbiont relationships are ubiquitous in nature, yet evolutionary and ecological processes that shape these intricate associations are often poorly understood. All orders of birds engage in symbioses with feather mites, which are ectosymbiotic arthropods that spend their entire life on hosts. Due to their permanent obligatory association with hosts, limited dispersal and primarily vertical transmission, we hypothesized that the cospeciation between feather mites and hosts within one avian family (Parulidae) would be perfect (strict cospeciation). We assessed cophylogenetic patterns and tested for congruence between species in two confamiliar feather mite genera (Proctophyllodidae: Proctophyllodes, Amerodectes) found on 13 species of migratory warblers (and one other closely related migratory species) in the eastern United States. Based on COI sequence data, we found three Proctophyllodes lineages and six Amerodectes lineages. Distance‐ and event‐based cophylogenetic analyses suggested different cophylogenetic trajectories of the two mite genera, and although some associations were significant, there was little overall evidence supporting strict cospeciation. Host switching is likely responsible for incongruent phylogenies. In one case, we documented prairie warblers Setophaga discolor harboring two mite species of the same genus. Most interestingly, we found strong evidence that host ecology may influence the likelihood of host switching occurring. For example, we documented relatively distantly related ground‐nesting hosts (ovenbird Seiurus aurocapilla and Kentucky warbler Geothlypis formosa) sharing a single mite species, while other birds are shrub/canopy or cavity nesters. Overall, our results suggest that cospeciation is not the case for feather mites and parulid hosts at this fine phylogenetic scale, and raise the question if cospeciation applies for other symbiotic systems involving hosts that have complex life histories. We also provide preliminary evidence that incorporating host ecological traits into cophylogenetic analyses may be useful for understanding how symbiotic systems have evolved.