Host space, not energy or symbiont size, constrains feather mite abundance across passerine bird species.

Comprehending symbiont abundance among host species is a major ecological endeavour, and the metabolic theory of ecology has been proposed to understand what constrains symbiont populations. We parameterized metabolic theory equations to investigate how bird species' body size and the body size of their feather mites relate to mite abundance according to four potential energy (uropygial gland size) and space constraints (wing area, total length of barbs and number of feather barbs). Predictions were compared with the empirical scaling of feather mite abundance across 106 passerine bird species (26,604 individual birds sampled), using phylogenetic modelling and quantile regression. Feather mite abundance was strongly constrained by host space (number of feather barbs) but not by energy. Moreover, feather mite species' body size was unrelated to the body size of their host species. We discuss the implications of our results for our understanding of the bird-feather mite system and for symbiont abundance in general.

Quantitative Interspecific Approach to the Stylosphere: Patterns of Bacteria and Fungi Abundance on Passerine Bird Feathers.

Feathers are the habitat of a myriad of organisms, from fungi and bacteria to lice and mites. Although most studies focus on specific taxa and their interaction with the bird host, anecdotal data glimpse feathers as holders of a system with its own ecology, what we call here the stylosphere. A major gap in our knowledge of the stylosphere is the ecology of the total abundance of microorganisms, being also rare to find studies that analyze abundance of more than one group of microorganisms at the bird interspecific level. Here, we quantified bacterial and fungi abundances through qPCR on the wing feathers of 144 birds from 24 passerine and one non-passerine bird species from three localities in Southern Spain. Bacteria and fungi abundances spanned three orders of magnitude among individual birds, but were consistent when comparing the right and the left wing feathers of individuals. Sampling locality explained ca. 14% of the variation in both bacteria and fungi abundances. Even when statistically controlling for sampling locality, microbial abundances consistently differed between birds from different species, but these differences were not explained by bird phylogeny. Finally, bird individuals and species having more bacteria also tended to held larger abundances of fungi. Our results suggest a quite complex explanation for stylosphere microorganisms' abundance, being shaped by bird individual and species traits, as well as environmental factors, and likely bacteria-fungi interactions.

Persistence of single species of symbionts across multiple closely-related host species.

Some symbiont species are highly host-specific, inhabiting only one or a very few host species, and typically have limited dispersal abilities. When they do occur on multiple host species, populations of such symbionts are expected to become genetically structured across these different host species, and this may eventually lead to new symbiont species over evolutionary timescales. However, a low number of dispersal events of symbionts between host species across time might be enough to prevent population structure and species divergence. Overall, processes of evolutionary divergence and the species status of most putative multi-host symbiont systems are yet to be investigated. Here, we used DNA metabarcoding data of 6,023 feather mites (a total of 2,225 OTU representative sequences) from 147 infracommunities (i.e., the assemblage consisting of all mites of different species collected from the same bird host individual) to investigate patterns of population genetic structure and species status of three different putative multi-host feather mite species Proctophyllodes macedo Vitzthum, 1922, Proctophyllodes motacillae Gaud, 1953, and Trouessartia jedliczkai (Zimmerman, 1894), each of which inhabits a variable number of different closely related wagtail host species (genus Motacilla). We show that mite populations from different host species represent a single species. This pattern was found in all the mite species, suggesting that each of these species is a multi-host species in which dispersal of mites among host species prevents species divergence. Also, we found evidence of limited evolutionary divergence manifested by a low but significant level of population genetic structure among symbiont populations inhabiting different host species. Our study agrees with previous studies showing a higher than expected colonization opportunities in host-specific symbionts. Indeed, our results support that these dispersal events would allow the persistence of multi-host species even in symbionts with limited dispersal capabilities, though additional factors such as the geographical structure of some bird populations may also play a role.

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.

Unexpected bird-feather mite associations revealed by DNA metabarcoding uncovers a dynamic ecoevolutionary scenario.

The high relevance of host-switching for the diversification of highly host-specific symbionts (i.e., those commonly inhabiting a single host species) demands a better understanding of host-switching dynamics at an ecological scale. Here, we used DNA metabarcoding to study feather mites on passerine birds in Spain, sequencing mtDNA (COI) for 25,540 individual mites (representing 64 species) from 1,130 birds (representing 71 species). Surprisingly, 1,228 (4.8%) mites from 84 (7.4%) birds were found on host species that were not the expected to be a host according to a recent bird-feather mite associations catalog. Unexpected associations were widespread across studied mite (40.6%) and bird (43.7%) species and showed smaller average infrapopulation sizes than typical associations. Unexpected mite species colonized hosts being distantly related to the set of their usual hosts, but with similar body size. The network of bird-mite associations was modular (i.e., some groups of bird and mite species tended to be more associated with each other than with the others), with 75.9% of the unexpected associations appearing within the module of the typical hosts of the mite species. Lastly, 68.4% of mite species found on unexpected hosts showed signatures of genetic differentiation, and we found evidence for reproduction or the potential for it in many of the unexpected associations. Results show host colonization as a common phenomenon even for these putatively highly host-specific symbionts. Thus, host-switching by feather mites, rather than a rare phenomenon, appears as a relatively frequent phenomenon shaped by ecological filters such as host morphology and is revealed as a fundamental component for a dynamic coevolutionary and codiversification scenario.

Enabling large-scale feather mite studies: an Illumina DNA metabarcoding pipeline.

Feather mites are among the most common and diverse ectosymbionts of birds, yet basic questions such as the nature of their relationship remain largely unanswered. One reason for feather mites being understudied is that their morphological identification is often virtually impossible when using female or young individuals. Even for adult male specimens this task is tedious and requires advanced taxonomic expertise, thus hampering large-scale studies. In addition, molecular-based methods are challenging because the low DNA amounts usually obtained from these tiny mites do not reach the levels required for high-throughput sequencing. This work aims to overcome these issues by using a DNA metabarcoding approach to accurately identify and quantify the feather mite species present in a sample. DNA metabarcoding is a widely used molecular technique that takes advantage of high-throughput sequencing methodologies to assign the taxonomic identity to all the organisms present in a complex sample (i.e., a sample made up of multiple specimens that are hard or impossible to individualise). We present a high-throughput method for feather mite identification using a fragment of the COI gene as marker and Illumina Miseq technology. We tested this method by performing two experiments plus a field test over a total of 11,861 individual mites (5360 of which were also morphologically identified). In the first experiment, we tested the probability of detecting a single feather mite in a heterogeneous pool of non-conspecific individuals. In the second experiment, we made 2 × 2 combinations of species and studied the relationship between the proportion of individuals of a given species in a sample and the proportion of sequences retrieved to test whether DNA metabarcoding can reliably quantify the relative abundance of mites in a sample. Here we also tested the efficacy of degenerate primers (i.e., a mixture of similar primers that differ in one or several bases that are designed to increase the chance of annealing) and investigated the relationship between the number of mismatches and PCR success. Finally, we applied our DNA metabarcoding pipeline to a total of 6501 unidentified and unsorted feather mite individuals sampled from 380 European passerine birds belonging to 10 bird species (field test). Our results show that this proposed pipeline is suitable for correct identification and quantitative estimation of the relative abundance of feather mite species in complex samples, especially when dealing with a moderate number (> 30) of individuals per sample.

Evidence of cryptic species in the genus Tinaminyssus (Acari: Rhinonyssidae) based on morphometrical and molecular data.

The study of cryptic species allows to describe and to understand biodiversity, and the evolutionary processes shaping it. Mites of the family Rhinonyssidae are permanent parasites of the nasal cavities of birds, currently including about 500 described species and 12 genera. Here, we tested the hypothesis that mites from five populations of the genus Tinaminyssus-three isolated from European turtle doves (Streptopelia turtur), and two from Eurasian collared doves (Streptopelia decaocto; Aves: Columbiformes)-are, in fact, two cryptic species inhabiting different hosts. First, we performed a morphometrical study on 16 traits. Then, we used the ITS1-5.8S rDNA-ITS2 nuclear region (ITS region), and a fragment of the mitochondrial cytochrome c-oxidase 1 (COI) to carry out phylogenetic and species delimitation analyses on Tinaminyssus species. Morphological analyses revealed a lack of biometric differentiation among Tinaminyssus populations from the two host species. However, molecular analyses indicated a high degree of genetic differentiation between populations of Tinaminyssus sp. from S. turtur and S. decaocto. Overall, results show that they can be considered as different cryptic species, suggesting a case of evolutionary stasis, likely because of the anatomical similarity between closely-related bird host species.

The complete mitochondrial genome of the feather mite Trouessartia rubecula Jablonska, 1968 (Astigmata: Analgoidea: Trouessartiidae).

We assembled and annotated the complete mitochondrial genome of Trouessartia rubecula, the first feather mite complete mitochondrial genome from the largest feather mite superfamily Analgoidea (ca. 1150 spp). The mitogenome was composed of 13 protein, 17 tRNA, and 2 rRNA-coding genes and was 14,125 bp in length.

Should I Change or Should I Go? Phenotypic Plasticity and Matching Habitat Choice in the Adaptation to Environmental Heterogeneity.

It can be challenging for organisms to achieve a good match between their phenotypic characteristics and environmental requirements that vary in space and time. The evolution of adaptive phenotypes can result from genetic differentiation at the population level. Individuals, however, could also change their phenotype (adaptive plasticity) or select an environment because it matches with their phenotype (matching habitat choice). It is poorly known under which conditions these different solutions to environmental heterogeneity evolve and whether they operate together. Using an individual-based simulation model, we assessed which solutions evolved depending on degree of temporal variation, costs of multiple underlying traits, and order of dispersal and development. Population genetic divergence was superseded by plasticity or matching habitat choice as temporal variation increased. Plasticity and matching habitat choice were limited by their trait costs, even when this involved only a part of the underlying traits. Independent of the order of dispersal and development, plasticity evolved more commonly than matching habitat choice, in part because the match a phenotype can achieve by matching habitat choice is limited by the types of environments available. Our results explain the apparent relative rarity of matching habitat choice in nature. At the same time, our results can be used to look for matching habitat choice in those biological systems where the conditions for other solutions seem unfavorable.

Parasite biodiversity faces extinction and redistribution in a changing climate.

Climate change is a well-documented driver of both wildlife extinction and disease emergence, but the negative impacts of climate change on parasite diversity are undocumented. We compiled the most comprehensive spatially explicit data set available for parasites, projected range shifts in a changing climate, and estimated extinction rates for eight major parasite clades. On the basis of 53,133 occurrences capturing the geographic ranges of 457 parasite species, conservative model projections suggest that 5 to 10% of these species are committed to extinction by 2070 from climate-driven habitat loss alone. We find no evidence that parasites with zoonotic potential have a significantly higher potential to gain range in a changing climate, but we do find that ectoparasites (especially ticks) fare disproportionately worse than endoparasites. Accounting for host-driven coextinctions, models predict that up to 30% of parasitic worms are committed to extinction, driven by a combination of direct and indirect pressures. Despite high local extinction rates, parasite richness could still increase by an order of magnitude in some places, because species successfully tracking climate change invade temperate ecosystems and replace native species with unpredictable ecological consequences.

Cophylogenetic analyses reveal extensive host-shift speciation in a highly specialized and host-specific symbiont system.

Host-shift speciation and cospeciation are the two major processes driving symbiont macroevolutionary diversification. Cospeciation is expected to be frequent in vertically transmitted and host-specific symbionts, and leads to congruent host-symbiont phylogenies. However, the cophylogenetic dynamics of many groups of highly specialized host-specific symbionts is largely unstudied. Thus, the relevance of cospeciation vs. host-shift speciation remains largely unknown. Here, we investigated this question by performing the largest cophylogenetic study of feather mites to date, using both distance and event-based cophylogenetic methods. For these analyses, we inferred phylogenies based on all protein coding genes of the mitochondrial genome of Proctophyllodes and Trouessartia feather mite species living on European passerine birds. Results show high incongruence among bird and feather mite phylogenies, because of extensive host-switching. We conclude that host-shift speciation, rather than cospeciation, may be the main driver of symbiont diversification even for highly specialized symbionts with low host-switching potential.

Shape matters: animal colour patterns as signals of individual quality.

Colour patterns (e.g. irregular, spotted or barred forms) are widespread in the animal kingdom, yet their potential role as signals of quality has been mostly neglected. However, a review of the published literature reveals that pattern itself (irrespective of its size or colour intensity) is a promising signal of individual quality across species of many different taxa. We propose at least four main pathways whereby patterns may reliably reflect individual quality: (i) as conventional signals of status, (ii) as indices of developmental homeostasis, (iii) by amplifying cues of somatic integrity and (iv) by amplifying individual investment in maintenance activities. Methodological constraints have traditionally hampered research on the signalling potential of colour patterns. To overcome this, we report a series of tools (e.g. colour adjacency and pattern regularity analyses, Fourier and granularity approaches, fractal geometry, geometric morphometrics) that allow objective quantification of pattern variability. We discuss how information provided by these methods should consider the visual system of the model species and behavioural responses to pattern metrics, in order to allow biologically meaningful conclusions. Finally, we propose future challenges in this research area that will require a multidisciplinary approach, bringing together inputs from genetics, physiology, behavioural ecology and evolutionary-developmental biology.

Fault bars in bird feathers: mechanisms, and ecological and evolutionary causes and consequences.

Fault bars are narrow malformations in feathers oriented almost perpendicular to the rachis where the feather vein and even the rachis may break. Breaks in the barbs and barbules result in small pieces of the feather vein being lost, while breaks in the rachis result in loss of the distal portion of the feather. Here, we provide a comprehensive review of 74 papers on fault bar formation in hopes of providing a clearer approach to their study. First, we review the evidence that the propensity to develop fault bars is modified by natural selection. Given that fault bars persist in the face of survival costs, we conclude that they must be an unfortunate consequence of some alternative adaptation that outweighs the fitness costs of fault bars. Second, we summarize evidence that the development of fault bars is triggered by psychological stress such as that of handling or predation attempts, and that they persist because the sudden contractions of the muscles in the feather follicle that control fright moults also causes the development of fault bars in growing feathers. Third, we review external and physiological (e.g. corticosterone) agents that may affect the likelihood that an acute stress will result in a growing feather exhibiting a fault bar. These modifying factors have often been treated as fundamental causes in the earlier literature on fault bars. Fourth, we then use this classification to propose a tentative model where fault bars of different severity (from light to severe) are the outcome of the interaction between the propensity to produce fault bars (which differs between species, individuals and feather follicles within individuals) and the intensity of the perturbation. This model helps to explain contradictory results in the literature, to identify gaps in our knowledge, and to suggest further studies. Lastly, we discuss ways in which better understanding of fault bars can inform us about other aspects of avian evolutionary ecology, such as the physiology of moult, the integration of moult into avian life cycles, and the strategies used to minimize stress during moult. Moreover, the study of fault bars may be relevant to understanding the aerodynamics of flight and the early evolution of flight.

Global associations between birds and vane-dwelling feather mites.

Understanding host-symbiont networks is a major question in evolutionary ecology. Birds host a great diversity of endo- and ectosymbiotic organisms, with feather mites (Arachnida: Acariformes: Analgoidea, Pterolichoidea) being among the most diverse of avian symbionts. A global approach to the ecology and evolution of bird-feather-mite associations has been hampered because of the absence of a centralized data repository. Here we present the most extensive data set of associations between feather mites and birds. Data include 12 036 records of 1887 feather mite species located on the flight feathers of 2234 bird species from 147 countries. Feather mites typically located inside quills, on the skin, or on downy body feathers are not included. Data were extracted from 493 published sources dating from 1882 to 2015. Data exploration shows that although most continents and bird families are represented, most bird species remain unexplored for feather mites. Nevertheless, this is the most comprehensive data set available for enabling global macroecological analyses of feather mites and their hosts, such as ecological network analyses. This metadata file outlines the structure of these data and provides primary references for all records used.

DNA barcoding of Iberian Peninsula and North Africa Tawny Owls Strix aluco suggests the Strait of Gibraltar as an important barrier for phylogeography.

Eight subspecies have been proposed within the Tawny Owl (Strix aluco) species. However, recent molecular data have challenged this view, encouraging further work in this species complex. Here we reevaluated the taxonomic status between the North-Western African Tawny Owl, S. a. mauritanica, and its closest Iberian Tawny Owl population (from the S. a. sylvatica to S. a. aluco clade) separated by the Strait of Gibraltar. The Tawny Owl is a non-migratory and territorial species, and juvenile dispersal is restricted to a few kilometers around the natal site. This limited dispersal and the barrier imposed by the Strait of Gibraltar predicted a strong differentiation between the two populations. We tested this using DNA barcoding, Bayesian phylogenetic and species delimitation analysis. We found that an 81.1% of variation is due to the intergroups variation. In addition, the inter-intraspecific distances distribution revealed a barcoding gap among the two subspecies. Also, posterior probabilities and the PAB value allowed to reject the hypothesis that observed degree of distinctiveness is due to random coalescence processes. These findings clearly support the Strait of Gibraltar as an isolating barrier for this species. The subspecific status is confirmed and species status is even suggested for S. a. mauritanica.

A new feather mite of the genus Dolichodectes (Astigmata: Proctophyllodidae) from Hippolais polyglotta (Passeriformes: Acrocephalidae) in Spain.

A new feather mite species, Dolichodectes hispanicus sp. n. (Astigmata: Proctophyllodidae), is described from the Melodious Warbler Hippolais polyglotta (Vieillot) (Passeriformes: Acrocephalidae) in Spain. The new species is closest to the type species of the genus, D. edwardsi (Trouessart, 1885) from the Grear Reed-Warbler Acrocephalus arundinaceus (Linnaeus) (Acrocephalidae). Adults of D. hispanicus differ from those of D. edwardsi by dimensional characteristics, in particular, by having shorter aedeagus that does not extend to the anal suckers in males and shorter hysteronotal shield in females. Tritonymphs of D. hispanicus are much more distinctive and differ from those of D. edwardsi by having the prodorsal shield covering all the prodorsum, the hysteronotal shield occupying about three quarters of the hysterosoma, and idiosomal setae h3 being filiform. The morphological description of the new species is augmented by sequence data from the mitochondrial cytochrome c oxidase subunit I gene fragment (COI).

DNA barcoding and minibarcoding as a powerful tool for feather mite studies.

Feather mites (Astigmata: Analgoidea and Pterolichoidea) are among the most abundant and commonly occurring bird ectosymbionts. Basic questions on the ecology and evolution of feather mites remain unanswered because feather mite species identification is often only possible for adult males, and it is laborious even for specialized taxonomists, thus precluding large-scale identifications. Here, we tested DNA barcoding as a useful molecular tool to identify feather mites from passerine birds. Three hundred and sixty-one specimens of 72 species of feather mites from 68 species of European passerine birds from Russia and Spain were barcoded. The accuracy of barcoding and minibarcoding was tested. Moreover, threshold choice (a controversial issue in barcoding studies) was also explored in a new way, by calculating through simulations the effect of sampling effort (in species number and species composition) on threshold calculations. We found one 200-bp minibarcode region that showed the same accuracy as the full-length barcode (602 bp) and was surrounded by conserved regions potentially useful for group-specific degenerate primers. Species identification accuracy was perfect (100%) but decreased when singletons or species of the Proctophyllodes pinnatus group were included. In fact, barcoding confirmed previous taxonomic issues within the P. pinnatus group. Following an integrative taxonomy approach, we compared our barcode study with previous taxonomic knowledge on feather mites, discovering three new putative cryptic species and validating three previous morphologically different (but still undescribed) new species.