Influence of host ecology and morphology on the diversity of Neotropical bird lice

Host‐parasite systems can be powerful arenas in which to explore factors influencing community structure. We used a comparative approach to examine the influence of host ecology and morphology on the diversity of chewing lice (Insecta: Phthiraptera) among 52 species of Peruvian birds. For each host species we calculated two components of parasite diversity: 1) cumulative species richness, and 2) mean abundance. We tested for correlations between these parasite indices and 13 host ecological and morphological variables. Host ecological variables included geographic range size, local population density, and microhabitat use. Host morphological variables included body mass, plumage depth, and standard dimensions of bill, foot and toenail morphology, all of which could influence the efficiency of anti‐parasite grooming. Data were analysed using statistical and comparative methods that control for sampling effort and host phylogeny. None of the independent host variables correlated with louse species richness when treated as a dependent variable. When richness was treated as an independent variable, however, it was positively correlated with mean louse abundance. Host body mass was also positively correlated with mean louse abundance. When louse richness and host body mass were held constant, mean louse abundance correlated negatively with the degree to which the upper mandible of the host's bill overhangs the lower mandible. This correlation suggests that birds with longer overhangs are better at controlling lice during preening. We propose a specific functional hypothesis in which preening damages lice by exerting a shearing force between the overhang and the tip of the lower mandible. This study is the first to suggest a parasite‐control function of such a detailed component of bill morphology across species. Avian biologists have traditionally focused almost exclusively on bills as tools for feeding. We suggest that the adaptive radiation of bill morphology should be reinterpreted with both preening and feeding in mind.     

Identifying hotspots of parasite diversity from species–area relationships: host phylogeny versus host ecology

Interspecific variation in parasite species richness among host species has generated much empirical research. As in comparisons among geographical areas, controlling for variation in host body size is crucial because host size determines resource availability. Recent developments in the use of species–area relationships (SARs) to detect hotspots of biodiversity provide a powerful way to control for host body size, and to identify ‘hot’ and ‘cold hosts’ of parasite diversity, i.e. hosts with more or fewer parasites than expected from their size. Applying SAR modelling to six large datasets on parasite species richness in vertebrates, we search for hot and cold hosts and assess the effect of other ecological variables on the probability that a host species is hot/cold taking body size (and sampling effort) into account. Five non‐sigmoid SAR models were fitted to the data by optimisation; their relative likelihood was evaluated using the Bayesian information criterion, before deriving an averaged SAR function. Overall, the fit between the five SAR models and the actual data was poor; there was substantial uncertainty surrounding the fitted models, and the best model differed among the six datasets. These results show that host body size is not a strong or consistent determinant of parasite species richness across taxa. Hotspots were defined as host species lying above the upper limit of the 80% confidence interval of the averaged SAR, and coldspots as species lying below its lower limit. Our analyses revealed (1) no apparent effect of specific ecological factors (i.e. water temperature, mean depth range, latitude or population density) on the likelihood of a host species being a hot or coldspot; (2) evidence of phylogenetic clustering, i.e. hosts from certain families are more likely to be hotspots (or coldspots) than other species, independently of body size. These findings suggest that host phylogeny may sometimes outweigh specific host ecological traits as a predictor of whether or not a host species harbours more (or fewer) parasite species than expected for its size.     

Clever birds are lousy: co-variation between avian innovation and the taxonomic richness of their amblyceran lice

Lice (Insecta: Phthiraptera) are ectoparasites that reduce host life expectancy and sexual attractiveness. Their taxonomic richness varies considerably among their hosts. Previous studies have already explored some important factors shaping louse diversity. An unexplored potential correlate of louse taxonomic richness is host behavioural flexibility. In this comparative study, we examine the relationship between louse generic richness, innovative capabilities (as a proxy for behavioural flexibility), and brain size while controlling for host species diversity, phylogeny, body size and research effort. Using data for 108 avian families, we found a highly significant positive relationship between host innovative capabilities and the taxonomic richness of amblyceran lice, but a lack of a similar relationship in ischnoceran lice. Host brain size had only a marginal impact on amblyceran diversity and no correlation with ischnoceran diversity. This suggests that the effect in Amblycera is not mediated by metabolic limitations due to the energetic costs of brain size and maintenance, rather directly caused by the ecological differences between hosts with differing cognitive capabilities. We propose four alternative and mutually non-exclusive hypotheses that may explain this phenomenon.     

A hitchhikers guide to the Galápagos: co-phylogeography of Galápagos mockingbirds and their parasites

Background

Parasites are evolutionary hitchhikers whose phylogenies often track the evolutionary history of their hosts. Incongruence in the evolutionary history of closely associated lineages can be explained through a variety of possible events including host switching and host independent speciation. However, in recently diverged lineages stochastic population processes, such as retention of ancestral polymorphism or secondary contact, can also explain discordant genealogies, even in fully co-speciating taxa. The relatively simple biogeographic arrangement of the Galápagos archipelago, compared with mainland biomes, provides a framework to identify stochastic and evolutionary informative components of genealogic data in these recently diverged organisms.

Results

Mitochondrial DNA sequences were obtained for four species of Galápagos mockingbirds and three sympatric species of ectoparasites - two louse and one mite species. These data were complemented with nuclear EF1α sequences in selected samples of parasites and with information from microsatellite loci in the mockingbirds. Mitochondrial sequence data revealed differences in population genetic diversity between all taxa and varying degrees of topological congruence between host and parasite lineages. A very low level of genetic variability and lack of congruence was found in one of the louse parasites, which was excluded from subsequent joint analysis of mitochondrial data. The reconciled multi-species tree obtained from the analysis is congruent with both the nuclear data and the geological history of the islands.

Conclusions

The gene genealogies of Galápagos mockingbirds and two of their ectoparasites show strong phylogeographic correlations, with instances of incongruence mostly explained by ancestral genetic polymorphism. A third parasite genealogy shows low levels of genetic diversity and little evidence of co-phylogeny with their hosts. These differences can mostly be explained by variation in life-history characteristics, primarily host specificity and dispersal capabilities. We show that pooling genetic data from organisms living in close ecological association reveals a more accurate phylogeographic history for these taxa. Our results have implications for the conservation and taxonomy of Galápagos mockingbirds and their parasites.     

Size matters for lice on birds: Coevolutionary allometry of host and parasite body size

Body size is one of the most fundamental characteristics of all organisms. It influences physiology, morphology, behavior, and even interspecific interactions such as those between parasites and their hosts. Host body size influences the magnitude and variability of parasite size according to Harrison's rule (HR: positive relationship between host and parasite body sizes) and Poulin's Increasing Variance Hypothesis (PIVH: positive relationship between host body size and the variability of parasite body size). We analyzed parasite–host body size allometry for 581 species of avian lice (～15% of known diversity) and their hosts. We applied phylogenetic generalized least squares (PGLS) methods to account for phylogenetic nonindependence controlling for host and parasite phylogenies separately and variance heterogeneity. We tested HR and PIVH for the major families of avian lice (Ricinidae, Menoponidae, Philopteridae), and for distinct ecological guilds within Philopteridae. Our data indicate that most families and guilds of avian lice follow both HR and PIVH; however, ricinids did not follow PIVH and the “body lice” guild of philopterid lice did not follow HR or PIVH. We discuss mathematical and ecological factors that may be responsible for these patterns, and we discuss the potential pervasiveness of these relationships among all parasites on Earth.     

Helminth parasite richness among vertebrates

The numbers of intestinal helminth species (parasite richnesS) recorded from each of 488 vertebrate host species are compared using data compiled from the published literature. Associations between parasite richness, sampling effort, host size and host habitat (aquatic versus terrestrial) are assessed using a method designed to control for phylogenetic association. Parasite richness increases with the number of surveys on which each estimate of parasite richness is based (sampling effort). When the effects of sampling effort are controlled for, there remains a strong positive relationship between parasite richness and host body size. There is no tendency for aquatic hosts to harbour more parasite species than terrestrial hosts independently of differences in sampling effort and body size. The results are interpreted in the context of hosts representing habitats for parasite colonization, resource allocation between parasite species, and the age of the major mammalian radiations.     

Climate,host phylogeny and the connectivity of host communities govern regional parasite assembly

Aim

Identifying barriers that govern parasite community assembly and parasite invasion risk is critical to understand how shifting host ranges impact disease emergence. We studied regional variation in the phylogenetic compositions of bird species and their blood parasites (Plasmodium and Haemoproteus spp.) to identify barriers that shape parasite community assembly.

Location

Australasia and Oceania.

Methods

We used a data set of parasite infections from >10,000 host individuals sampled across 29 bioregions. Hierarchical models and matrix regressions were used to assess the relative influences of interspecies (host community connectivity and local phylogenetic distinctiveness), climate and geographic barriers on parasite local distinctiveness and composition.

Results

Parasites were more locally distinct (co‐occurred with distantly related parasites) when infecting locally distinct hosts, but less distinct (co‐occurred with closely related parasites) in areas with increased host diversity and community connectivity (a proxy for parasite dispersal potential). Turnover and the phylogenetic symmetry of parasite communities were jointly driven by host turnover, climate similarity and geographic distance.

Main conclusions

Interspecies barriers linked to host phylogeny and dispersal shape parasite assembly, perhaps by limiting parasite establishment or local diversification. Infecting hosts that co‐occur with few related species decreases a parasite's likelihood of encountering related competitors, perhaps increasing invasion potential but decreasing diversification opportunity. While climate partially constrains parasite distributions, future host range expansions that spread distinct parasites and diminish barriers to host shifting will likely be key drivers of parasite invasions.     

中国云南部分小兽体表吸虱昆虫群落相似性及群落分类研究(英文)

应用系统聚类分析方法对云南省境内24种主要小型哺乳动物(小兽)体表吸虱昆虫群落相似性及群落分类进行了研究。研究中将每一种小兽体表的所有吸虱昆虫定义为一个相应的吸虱群落单位。结果表明,小兽体表吸虱群落结构简单,物种多样性很低。多数小兽有固定的吸虱种类寄生,其吸虱的宿主特异性高。在动物分类上隶属同一个属的小兽,其体表吸虱群落相似程度高,在系统聚类分析中大多被归为一类。在动物分类上近缘的小兽,其体表吸虱群落相似,优势虱种相同或相似,此情形尤其表现在鼠属、白腹鼠属、姬鼠属和绒鼠属。吸虱群落相似性大小与相应小兽宿主在动物分类地位上的近缘性高低呈现高度一致。从生态学角度来看,吸虱昆虫与其所寄生的小兽宿主动物之间存在密切的协同进化关系。     

Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density

Aim  Comparative studies have revealed strong links between ecological factors and the number of parasite species harboured by different hosts, but studies of different taxonomic host groups have produced inconsistent results. As a step towards understanding the general patterns of parasite species richness, we present results from a new comprehensive data base of over 7000 host–parasite combinations representing 146 species of carnivores (Mammalia: Carnivora) and 980 species of parasites.
Methods  We used both phylogenetic and non-phylogenetic comparative methods while controlling for unequal sampling effort within a multivariate framework to ascertain the main determinants of parasite species richness in carnivores.
Results  We found that body mass, population density, geographical range size and distance from the equator are correlated with overall parasite species richness in fissiped carnivores. When parasites are classified by transmission mode, body mass and home range area are the main determinants of the richness of parasites spread by close contact between hosts, and population density, geographical range size and distance from the equator account for the diversity of parasites that are not dependent on close contact. For generalist parasites, population density, geographical range size and latitude are the primary predictors of parasite species richness. We found no significant ecological correlates for the richness of specialist or vector-borne parasites.
Main conclusions  Although we found that parasite species richness increases instead of decreases with distance from the equator, other comparative patterns in carnivores support previous findings in primates, suggesting that similar ecological factors operate in both these independent evolutionary lineages.     

Bat fly species richness in Neotropical bats: correlations with host ecology and host brain

Patterns of ectoparasite species richness in mammals have been investigated in various terrestrial mammalian taxa such as primates, ungulates and carnivores. Several ecological or life traits of hosts are expected to explain much of the variability in species richness of parasites. In the present comparative analysis we investigate some determinants of parasite richness in bats, a large and understudied group of flying mammals, and their obligate blood-sucking ectoparasite, streblid bat flies (Diptera). We investigate the effects of host body size, geographical range, group size and roosting ecology on the species richness of bat flies in tropical areas of Venezuela and Peru, where both host and parasite diversities are high. We use the data from a major sampling effort on 138 bat species from nine families. We also investigate potential correlation between bat fly species richness and brain size (corrected for body size) in these tropical bats. We expect a relationship if there is a potential energetic trade-off between costly large brains and parasite-mediated impacts. We show that body size and roosting in cavities are positively correlated with bat fly species richness. No effects of bat range size and group size were observed. Our results also suggest an association between body mass-independent brain size and bat fly species richness. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Local diversity reduces infection risk across multiple freshwater host‐parasite associations

相似文献   

Louse flies of Eleonora’s falcons that also feed on their prey are evolutionary dead‐end hosts for blood parasites

Host shifts are widespread among avian haemosporidians, although the success of transmission depends upon parasite‐host and parasite‐vector compatibility. Insular avifaunas are typically characterized by a low prevalence and diversity of haemosporidians, although the underlying ecological and evolutionary processes remain unclear. We investigated the parasite transmission network in an insular system formed by Eleonora's falcons (the avian host), louse flies that parasitize the falcons (the potential vector), and haemosporidians (the parasites). We found a great diversity of parasites in louse flies (16 Haemoproteus and 6 Plasmodium lineages) that did not match with lineages previously found infecting adult falcons (only one shared lineage). Because Eleonora's falcon feeds on migratory passerines hunted over the ocean, we sampled falcon kills in search of the origin of parasites found in louse flies. Surprisingly, louse flies shared 10 of the 18 different parasite lineages infecting falcon kills. Phylogenetic analyses revealed that all lineages found in louse flies (including five new lineages) corresponded to Haemoproteus and Plasmodium parasites infecting Passeriformes. We found molecular evidence of louse flies feeding on passerines hunted by falcons. The lack of infection in nestlings and the mismatch between the lineages isolated in adult falcons and louse flies suggest that despite louse flies’ contact with a diverse array of parasites, no successful transmission to Eleonora's falcon occurs. This could be due to the falcons’ resistance to infection, the inability of parasites to develop in these phylogenetically distant species, or the inability of haemosporidian lineages to complete their development in louse flies.     

Integrating phylogenomic and population genomic patterns in avian lice provides a more complete picture of parasite evolution

Parasite diversity accounts for most of the biodiversity on earth, and is shaped by many processes (e.g., cospeciation, host switching). To identify the effects of the processes that shape parasite diversity, it is ideal to incorporate both deep (phylogenetic) and shallow (population) perspectives. To this end, we developed a novel workflow to obtain phylogenetic and population genetic data from whole genome sequences of body lice parasitizing New World ground‐doves. Phylogenies from these data showed consistent, highly resolved species‐level relationships for the lice. By comparing the louse and ground‐dove phylogenies, we found that over long‐term evolutionary scales their phylogenies were largely congruent. Many louse lineages (both species and populations) also demonstrated high host‐specificity, suggesting ground‐dove divergence is a primary driver of their parasites’ diversity. However, the few louse taxa that are generalists are structured according to biogeography at the population level. This suggests dispersal among sympatric hosts has some effect on body louse diversity, but over deeper time scales the parasites eventually sort according to host species. Overall, our results demonstrate that multiple factors explain the patterns of diversity in this group of parasites, and that the effects of these factors can vary over different evolutionary scales. The integrative approach we employed was crucial for uncovering these patterns, and should be broadly applicable to other studies.     

Host traits and parasite species richness in even and odd-toed hoofed mammals, Artiodactyla and Perissodactyla

Host social, ecological and life history traits are predicted to influence both parasite establishment within host species and the distribution of parasites among host species. Yet only a few studies have investigated the role multiple host traits play in determining patterns of infection across diverse parasite groups. To explore the association between host traits and parasite species richness (PSR), we assembled a comprehensive database encompassing 601 parasites (including viruses, bacteria, protozoa, helminths and arthropods) reported to infect 96 species from two well-studied and diverse host clades: even- and odd-toed hoofed mammals (Artiodactyla and Perissodactyla). Comparative analyses were used to examine associations between three sets of host variables (life history and body mass, social and mating behavior, and ecological traits) and PSR for all parasites combined and for distinct parasite sub-groups. Results from a combination of phylogenetic and non-phylogenetic tests showed that PSR increased with host body size across all parasites groups. Counter to expectations, measures of parasite diversity decreased with host longevity and social group size, and associations between group size and PSR further depended on the underlying mating system of the host species. Our results suggest that body mass, longevity, and social organization influence the diversity and types of parasites reported to infect wild populations of hoofed mammals, and that multiple host and parasite traits can combine in unexpected ways to shape observed patterns.     

The role of body size in host specificity: reciprocal transfer experiments with feather lice

Although most parasites show at least some degree of host specificity, factors governing the evolution of specificity remain poorly understood. Many different groups of host-specific parasites show a striking correlation between parasite and host body size, suggesting that size reinforces specificity. We tested this hypothesis by measuring the relative fitness of host-specific feather lice transferred to pigeons and doves that differ in size by an order of magnitude. To test the general influence of size, we transferred unrelated groups of wing and body lice, which are specialized for different regions of the host. Lice were transferred in both directions, from a large native host species, the rock pigeon (Columba livia), to several progressively smaller hosts, and from a small native host species, the common ground dove (Columbina passerina), to several larger hosts. We measured the relative fitness (population size) of lice transferred to these novel host species after two louse generations. Neither wing lice nor body lice could survive on novel host species that were smaller in size than the native host. However, when host defense (preening behavior) was blocked, both groups survived and reproduced on all novel hosts tested. Thus, host defense interacted with host size to govern the ability of lice to establish on small hosts. Neither wing lice nor body lice could survive on larger hosts, even when preening was blocked. In summary, host size influenced the fitness of both types of feather lice, but through different mechanisms, depending on the direction of the transfer. Our results indicate that host switching is most likely between hosts of similar body size. This finding has important implications for studies of host-parasite coevolution at both the micro- and macroevolutionary scales.     

Small steps or giant leaps for male-killers? Phylogenetic constraints to male-killer host shifts

Background  

Arthropods are infected by a wide diversity of maternally transmitted microbes. Some of these manipulate host reproduction to facilitate population invasion and persistence. Such parasites transmit vertically on an ecological timescale, but rare horizontal transmission events have permitted colonisation of new species. Here we report the first systematic investigation into the influence of the phylogenetic distance between arthropod species on the potential for reproductive parasite interspecific transfer.     

Cryptic diversity and patterns of host specificity in trematode flatworms

The widespread utilization of molecular markers has revealed that a broad spectrum of taxa contain sets of morphologically cryptic, but genetically distinct lineages ( Bickford et al. 2007 ). The identification of cryptic taxa is important as an accurate appreciation of diversity is crucial for a proper understanding of evolutionary and ecological processes. An example is the study of host specificity in parasitic taxa, where an apparent generalist may be found to contain a complex of several more specific species ( Smith et al. 2006 ). Host specificity is a key life history trait that varies greatly among parasites ( Poulin & Keeney 2007 ). While some can exploit a wide range of hosts, others are confined to just a single species. Access to additional hosts increases the resources available to a parasite. However, physiological or ecological constraints can restrict the extension of host range. Furthermore, there may be a trade‐off between relaxed specificity and performance: generalism can decrease a parasites ability to adapt to each individual host species, and increase exposure to competition from other parasites ( Poulin 1998 ). Despite the central role that host specificity plays in parasite life history, relatively little is known about how host range is determined in natural systems, and data from field studies are required to evaluate among competing ideas. In this issue, an exciting paper by Locke et al. (2010) makes a valuable contribution toward the understanding of host specificity in an important group of trematode flatworms. Using molecular methods, Locke et al. reveal an almost four‐fold increase in the appreciated diversity of their focal group. In combination with a large and elegant sampling design this allows them to accurately assess host specificity for each taxon, and thus draw key insights into the factors that control host range in a dominant parasite group.     

SIMILARITY COMPARISON AND CLASSIFICATION OF SUCKING LOUSE COMMUNITIES ON SOME SMALL MAMMALS IN YUNNAN, CHINA

Abstract  The similarity and classification of sucking louse communities on 24 species of small mammals were studied in Yunnan Province, China, through a hierarchical cluster analysis. All the louse species on the body surface of a certain species of small mammals are regarded as a louse community unit. The results reveal that the community structure of sucking lice on small mammals is simple with low species diversity. Most small mammals usually have certain louse species on their body surface; there exists a high degree of host specificity. Most louse communities on the same genus of small mammals show a high similarity and are classified into the same group based on hierarchical cluster analysis. When the hosts have a close affinity in taxonomy, the louse communities on their body surface would tend to be similar with the same or similar dominant louse species (as observed in genus Rattus, Niviventer, Apodemus and Eothenomys ). The similarity of sucking louse communities is highly consistent with the affinity of small mammal hosts in taxonomy. The results suggest a close relationship of co-evolution between sucking lice and their hosts.     

Metazoan parasites of African annual killifish (Nothobranchiidae): abundance,diversity, and their environmental correlates

Estimates of biodiversity and its global patterns are affected by parasite richness and specificity. Despite this, parasite communities are largely neglected in biodiversity estimates, especially in the tropics. We studied the parasites of annual killifish of the genus Nothobranchius that inhabit annually desiccating pools across the African savannah and survive the dry period as developmentally arrested embryos. Their discontinuous, non‐overlapping generations make them a unique organism in which to study natural parasite fauna. We investigated the relationship between global (climate and altitude) and local (pool size, vegetation, host density and diversity, and diversity of potential intermediate hosts) environmental factors and the community structure of killifish parasites. We examined metazoan parasites from 21 populations of four host species (Nothobranchius orthonotus, N. furzeri, N. kadleci, and N. pienaari) across a gradient of aridity in Mozambique. Seventeen parasite taxa were recorded, with trematode larval stages (metacercariae) being the most abundant taxa. The parasites recorded were both allogenic (life cycle includes non‐aquatic host; predominantly trematodes) and autogenic (cycling only in aquatic hosts; nematodes). The parasite abundance was highest in climatic regions with intermediate aridity, while parasite diversity was associated with local environmental characteristics and positively correlated with fish species diversity and the amount of aquatic vegetation. Our results suggest that parasite communities of sympatric Nothobranchius species are similar and dominated by the larval stages of generalist parasites. Therefore, Nothobranchius serve as important intermediate or paratenic hosts of parasites, with piscivorous birds and predatory fish being their most likely definitive hosts.