Understanding the ecological function of species and the structure of communities is crucial in t... more Understanding the ecological function of species and the structure of communities is crucial in the study of ecological interactions among species. For this purpose, not only the occurrence of particular species but also their abundance in ecological communities is required. However, abundance quantification of species through morphological characters is often difficult or time/money consuming when dealing with elusive or small taxa. Here we tested the use of next-generation sequencing (NGS) for abundance estimation of two species of feather mites (Proctophyllodes stylifer and Pteronyssoides parinus) under five different proportions (16:1, 16:4, 16:16, 16:64, and 16 vs 256 mites) against a mock community composed by Proctophyllodes clavatus and Proctophyllodes sylviae. In all mixtures, we retrieved sequence reads from all species. We found a strong linear relationship between 454 reads and the real proportion of individuals in the mixture for both focal species. The slope for Pr. stylifer was close to one (0.904), and the intercept close to zero (-0.007), thus showing an almost perfect correspondence between real and estimated proportions. The slope for Pt. parinus was 0.351 and the intercept 0.307, showing that while the estimated proportion increased linearly relative to real proportions of individuals in the samples, proportions were overestimated at low real proportions and underestimated at larger ones. Additionally, pyrosequencing replicates from each DNA extraction were highly repeatable (R=0.920 and 0.972, respectively), showing that the quantification method is highly consistent given a DNA extract. Our study suggests that NGS is a promising tool for abundance estimation of feather mites' communities in birds.
Understanding the selective forces that shape genetic variation in natural populations remains a ... more Understanding the selective forces that shape genetic variation in natural populations remains a high priority in evolutionary biology. Genes at the major histocompatibility complex (MHC) have become excellent models for the investigation of adaptive variation and natural selection because of their crucial role in fighting off pathogens. Here we present one of the first data sets examining patterns of MHC variation in wild populations of a bird of prey, the lesser kestrel, Falco naumanni. We report extensive polymorphism at the second exon of a putatively functional MHC class II gene, Fana-DAB*1. Overall, 103 alleles were isolated from 121 individuals sampled from Spain to Kazakhstan. Bayesian inference of diversifying selection suggests that several amino acid sites may have experienced strong positive selection (ω = 4.02 per codon). The analysis also suggests a prominent role of recombination in generating and maintaining MHC diversity (ρ = 4Nc = 0.389 per codon, θ = 0.017 per codon). Both the Fana-DAB*1 locus and a set of eight polymorphic microsatellite markers revealed an isolation-by-distance pattern across the Western Palaearctic (r = 0.67; P = 0.01 and r = 0.50; P = 0.04, respectively). Nonetheless, geographical variation at the MHC contrasts with relatively uniform distributions in the frequencies of microsatellite alleles. In addition, we found lower fixation rates in the MHC than those predicted by genetic drift after controlling for neutral mitochondrial sequences. Our results therefore underscore the role of balancing selection as well as spatial variations in parasitemediated selection regimes in shaping MHC diversity when gene flow is limited.
1. The integration of capture-recapture and molecular approaches can improve our understanding of... more 1. The integration of capture-recapture and molecular approaches can improve our understanding of the consequences of habitat fragmentation on population connectivity. Here we employed microsatellites to test dispersal hypotheses derived from intense and long-term ringing programmes of the lesser kestrel Falco naumanni in Western Europe. 2. Re-encounters of 1308 marked individuals in Spain have revealed that most first-time breeders settled within 10 km from their natal colony, with a negative association between dispersal and geographical distance. Although these findings would predict fine-scale spatial patterns of genetic differentiation, the genetic impact of rarely reported events concerning long-distance effective dispersal (> 100 km) is unknown. 3. First, we investigated a spatially structured and geographically isolated population located in northeastern Spain, where capture-recapture records and genetic data could be appropriately compared over similar spatial and temporal scales. Spatial autocorrelation analyses (N = 174 nestlings from different broods) did not reveal either significant differences in average relatedness at any distance class nor decreased relatedness as a function of distance. At a broader spatial scale, Bayesian analysis of population structure (N = 432 nestlings) indicated panmixia across Western Europe. However, F ST comparisons between four geographically distinct populations indicated low but significant genetic differentiation. 4. Our genetic data would therefore challenge traditional assumptions associating philopatry with the emergence of fine-scale genetic structuring. This could be because even low levels of gene flow are enough to preclude the development of local genetic structure. Nevertheless, the analysis of a geographically isolated and small population from Southern France exemplifies a situation in which restricted dispersal has translated into weak but consistently significant genetic differentiation. 5. Relevant to conservation genetics and evolutionary biology, our results may lessen the genetic concerns derived from population fragmentation at relatively small geographical scales in species with apparently limited dispersal abilities, but raises concerns about increased genetic divergence in small and isolated demes.
We studied the mechanisms that regulate colony dynamics in a Spanish population of Lesser Kestrel... more We studied the mechanisms that regulate colony dynamics in a Spanish population of Lesser Kestrels, using eight years of data from banded individuals in 494 colony-years. Colony growth was positively related to breeding success at the colony the year before. However, individuals of all dispersal statuses, i.e., adult and first-breeding philopatric and immigrant birds, significantly contributed to changes in colony size, indicating an important effect of dispersal on colony dynamics via colony quality. Given that there is strong evidence that Lesser Kestrels base their settlement decisions on conspecifics, we tested whether immigrants used the number of previously settled residents in year t (social or conspecific attraction hypothesis) and/or the breeding performance of conspecifics in year t Ϫ 1 (performance-based attraction hypothesis) to select their breeding colony. Breeding success of colonies varied both in space and time and was autocorrelated from one year to the next. Moreover, lifetime reproductive success of Lesser Kestrels was positively associated with colony size, and individuals can predict final colony size early in the breeding season, so assumptions of both hypotheses were fulfilled. Our results support the social attraction hypothesis, since immigration was positively related to the number of philopatric adults, but not to conspecific breeding success the year before. Given that departure decisions of adults were based on personal information about breeding success and colony size is related to fitness prospects, previously settled individuals provide easy and reliable information about colony quality, and social attraction could be seen as a particular case of public information in Lesser Kestrels. Consistently, absolute numbers of both philopatric adults and immigrants increased with colony size the year before, although immigrants increased only up to a threshold beyond which this trend disappeared. Therefore, immigrants seem to be prevented from settling in the largest colonies, which could explain why all individuals do not concentrate in a few big colonies, but some settle in suboptimal colonies or colonize unoccupied sites. This opposing effect of conspecifics, together with the low levels of temporal autocorrelation in colony quality between time lags Ն2 yr, could promote colony size variability and facultative coloniality in this species.
Artificial nest experiments (ANEs) are widely used to obtain proxies of natural nest predation fo... more Artificial nest experiments (ANEs) are widely used to obtain proxies of natural nest predation for testing a variety of hypotheses, from those dealing with variation in life-history strategies to those assessing the effects of habitat fragmentation on the persistence of bird populations. However, their applicability to real-world scenarios has been criticized owing to the many potential biases in comparing predation rates of artificial and natural nests. Here, we aimed to test the validity of estimates of ANEs using a novel approach. We related predation rates on artificial nests to population viability analyses in a songbird metapopulation as a way of predicting the real impact of predation events on the local populations studied. Predation intensity on artificial nests was negatively related to the species' annual population growth rate in small local populations, whereas the viability of large local populations did not seem to be influenced, even by high nest predation rates....
Metapopulation theory is one of the most popular approaches to identify the factors affecting the... more Metapopulation theory is one of the most popular approaches to identify the factors affecting the spatial and temporal dynamics of populations in fragmented habitat networks. Habitat quality, patch area and isolation are mainly focused on when analyzing distribution patterns in fragmented landscapes. The effects of landscape heterogeneity in the non-occupied matrix, however, have been largely neglected. Here, we determined the relative importance of patch quality and landscape attributes on the occurrence, density and extinction of the Dupont's lark (Chersophilus duponti), an endangered steppe passerine whose habitat has been extremely reduced to highly isolated and fragmented patches embedded in a mainly unsuitable landscape matrix. Habitat patch quality, measured in terms of vegetation structure, grazing pressure, arthropod availability, predator abundance, and inter-specific competition, did not affect occurrence, density or extinction. At the landscape scale, however, the species' occurrence was principally determined by the interactions among patch size, geographic isolation and landscape matrix. Isolation had the main independent contribution to explaining the probability of occurrence, followed by landscape matrix composition and patch size. The species' density was negatively correlated to patch size, suggesting crowding effects in small fragments, while extinction events were exclusively related to isolation. Our findings suggest that landscape rather than local population characteristics are crucial in determining the patterns of distribution and abundance of non-equilibrium populations in highly fragmented habitat networks. Consequently, conservation measures for these species should simultaneously involve patch size, isolation and landscape matrix and apply to the entire metapopulation rather than to particular patches.
Animals attacked by predators often enter a state of tonic immobility (TI) in which individuals a... more Animals attacked by predators often enter a state of tonic immobility (TI) in which individuals appear to simulate death. Despite the fact that TI is often used as a proxy of fear in domesticated animals, quantitative data on individual variation is very scarce for wild vertebrates. As a consequence, we lack ecological interpretations for the variability in TI that may exist in wild populations. Here, we tested whether there are consistent differences among individuals in 2 components of TI within wild populations of 2 avian species, the Yellow-crowned bishop (Euplectes afer) and the Tree sparrow (Passer montanus). We next tested whether this variation reflects variation in boldness toward predators (measured as the response to 2 predator models) or is simply related to variation in general activity/restlessness (measured as baseline activity) in the bishop. We analyzed our data by means of Bayesian structural equation modeling (SEM), which has several general advantages and, moreover, allowed us to analyze censored (truncated) data. We found good support for relatively high repeatability within individuals of both components of TI. Measures of TI appeared to be uncorrelated with baseline activity. In contrast, our results suggest that individual variation in TI in a wild vertebrate can be interpreted in a context of boldness toward predators, making TI a meaningful and practical behavioral trait for studies involving personality and antipredation behavior in wild populations. In addition, we show that the Bayesian structural equation modeling approach to analyze censored data had greater statistical power than other approaches. Hence, this rarely implemented technique deserves to be more widely used.
The moult of birds could greatly perturb the life cycle of feather mites (Astigmata). These mites... more The moult of birds could greatly perturb the life cycle of feather mites (Astigmata). These mites live on the surface of feathers and are unlikely to survive if they are on one when it is moulted. Therefore, we hypothesized that they would escape to other feathers to avoid this ...
Understanding the ecological function of species and the structure of communities is crucial in t... more Understanding the ecological function of species and the structure of communities is crucial in the study of ecological interactions among species. For this purpose, not only the occurrence of particular species but also their abundance in ecological communities is required. However, abundance quantification of species through morphological characters is often difficult or time/money consuming when dealing with elusive or small taxa. Here we tested the use of next-generation sequencing (NGS) for abundance estimation of two species of feather mites (Proctophyllodes stylifer and Pteronyssoides parinus) under five different proportions (16:1, 16:4, 16:16, 16:64, and 16 vs 256 mites) against a mock community composed by Proctophyllodes clavatus and Proctophyllodes sylviae. In all mixtures, we retrieved sequence reads from all species. We found a strong linear relationship between 454 reads and the real proportion of individuals in the mixture for both focal species. The slope for Pr. stylifer was close to one (0.904), and the intercept close to zero (-0.007), thus showing an almost perfect correspondence between real and estimated proportions. The slope for Pt. parinus was 0.351 and the intercept 0.307, showing that while the estimated proportion increased linearly relative to real proportions of individuals in the samples, proportions were overestimated at low real proportions and underestimated at larger ones. Additionally, pyrosequencing replicates from each DNA extraction were highly repeatable (R=0.920 and 0.972, respectively), showing that the quantification method is highly consistent given a DNA extract. Our study suggests that NGS is a promising tool for abundance estimation of feather mites' communities in birds.
Understanding the selective forces that shape genetic variation in natural populations remains a ... more Understanding the selective forces that shape genetic variation in natural populations remains a high priority in evolutionary biology. Genes at the major histocompatibility complex (MHC) have become excellent models for the investigation of adaptive variation and natural selection because of their crucial role in fighting off pathogens. Here we present one of the first data sets examining patterns of MHC variation in wild populations of a bird of prey, the lesser kestrel, Falco naumanni. We report extensive polymorphism at the second exon of a putatively functional MHC class II gene, Fana-DAB*1. Overall, 103 alleles were isolated from 121 individuals sampled from Spain to Kazakhstan. Bayesian inference of diversifying selection suggests that several amino acid sites may have experienced strong positive selection (ω = 4.02 per codon). The analysis also suggests a prominent role of recombination in generating and maintaining MHC diversity (ρ = 4Nc = 0.389 per codon, θ = 0.017 per codon). Both the Fana-DAB*1 locus and a set of eight polymorphic microsatellite markers revealed an isolation-by-distance pattern across the Western Palaearctic (r = 0.67; P = 0.01 and r = 0.50; P = 0.04, respectively). Nonetheless, geographical variation at the MHC contrasts with relatively uniform distributions in the frequencies of microsatellite alleles. In addition, we found lower fixation rates in the MHC than those predicted by genetic drift after controlling for neutral mitochondrial sequences. Our results therefore underscore the role of balancing selection as well as spatial variations in parasitemediated selection regimes in shaping MHC diversity when gene flow is limited.
1. The integration of capture-recapture and molecular approaches can improve our understanding of... more 1. The integration of capture-recapture and molecular approaches can improve our understanding of the consequences of habitat fragmentation on population connectivity. Here we employed microsatellites to test dispersal hypotheses derived from intense and long-term ringing programmes of the lesser kestrel Falco naumanni in Western Europe. 2. Re-encounters of 1308 marked individuals in Spain have revealed that most first-time breeders settled within 10 km from their natal colony, with a negative association between dispersal and geographical distance. Although these findings would predict fine-scale spatial patterns of genetic differentiation, the genetic impact of rarely reported events concerning long-distance effective dispersal (> 100 km) is unknown. 3. First, we investigated a spatially structured and geographically isolated population located in northeastern Spain, where capture-recapture records and genetic data could be appropriately compared over similar spatial and temporal scales. Spatial autocorrelation analyses (N = 174 nestlings from different broods) did not reveal either significant differences in average relatedness at any distance class nor decreased relatedness as a function of distance. At a broader spatial scale, Bayesian analysis of population structure (N = 432 nestlings) indicated panmixia across Western Europe. However, F ST comparisons between four geographically distinct populations indicated low but significant genetic differentiation. 4. Our genetic data would therefore challenge traditional assumptions associating philopatry with the emergence of fine-scale genetic structuring. This could be because even low levels of gene flow are enough to preclude the development of local genetic structure. Nevertheless, the analysis of a geographically isolated and small population from Southern France exemplifies a situation in which restricted dispersal has translated into weak but consistently significant genetic differentiation. 5. Relevant to conservation genetics and evolutionary biology, our results may lessen the genetic concerns derived from population fragmentation at relatively small geographical scales in species with apparently limited dispersal abilities, but raises concerns about increased genetic divergence in small and isolated demes.
We studied the mechanisms that regulate colony dynamics in a Spanish population of Lesser Kestrel... more We studied the mechanisms that regulate colony dynamics in a Spanish population of Lesser Kestrels, using eight years of data from banded individuals in 494 colony-years. Colony growth was positively related to breeding success at the colony the year before. However, individuals of all dispersal statuses, i.e., adult and first-breeding philopatric and immigrant birds, significantly contributed to changes in colony size, indicating an important effect of dispersal on colony dynamics via colony quality. Given that there is strong evidence that Lesser Kestrels base their settlement decisions on conspecifics, we tested whether immigrants used the number of previously settled residents in year t (social or conspecific attraction hypothesis) and/or the breeding performance of conspecifics in year t Ϫ 1 (performance-based attraction hypothesis) to select their breeding colony. Breeding success of colonies varied both in space and time and was autocorrelated from one year to the next. Moreover, lifetime reproductive success of Lesser Kestrels was positively associated with colony size, and individuals can predict final colony size early in the breeding season, so assumptions of both hypotheses were fulfilled. Our results support the social attraction hypothesis, since immigration was positively related to the number of philopatric adults, but not to conspecific breeding success the year before. Given that departure decisions of adults were based on personal information about breeding success and colony size is related to fitness prospects, previously settled individuals provide easy and reliable information about colony quality, and social attraction could be seen as a particular case of public information in Lesser Kestrels. Consistently, absolute numbers of both philopatric adults and immigrants increased with colony size the year before, although immigrants increased only up to a threshold beyond which this trend disappeared. Therefore, immigrants seem to be prevented from settling in the largest colonies, which could explain why all individuals do not concentrate in a few big colonies, but some settle in suboptimal colonies or colonize unoccupied sites. This opposing effect of conspecifics, together with the low levels of temporal autocorrelation in colony quality between time lags Ն2 yr, could promote colony size variability and facultative coloniality in this species.
Artificial nest experiments (ANEs) are widely used to obtain proxies of natural nest predation fo... more Artificial nest experiments (ANEs) are widely used to obtain proxies of natural nest predation for testing a variety of hypotheses, from those dealing with variation in life-history strategies to those assessing the effects of habitat fragmentation on the persistence of bird populations. However, their applicability to real-world scenarios has been criticized owing to the many potential biases in comparing predation rates of artificial and natural nests. Here, we aimed to test the validity of estimates of ANEs using a novel approach. We related predation rates on artificial nests to population viability analyses in a songbird metapopulation as a way of predicting the real impact of predation events on the local populations studied. Predation intensity on artificial nests was negatively related to the species' annual population growth rate in small local populations, whereas the viability of large local populations did not seem to be influenced, even by high nest predation rates....
Metapopulation theory is one of the most popular approaches to identify the factors affecting the... more Metapopulation theory is one of the most popular approaches to identify the factors affecting the spatial and temporal dynamics of populations in fragmented habitat networks. Habitat quality, patch area and isolation are mainly focused on when analyzing distribution patterns in fragmented landscapes. The effects of landscape heterogeneity in the non-occupied matrix, however, have been largely neglected. Here, we determined the relative importance of patch quality and landscape attributes on the occurrence, density and extinction of the Dupont's lark (Chersophilus duponti), an endangered steppe passerine whose habitat has been extremely reduced to highly isolated and fragmented patches embedded in a mainly unsuitable landscape matrix. Habitat patch quality, measured in terms of vegetation structure, grazing pressure, arthropod availability, predator abundance, and inter-specific competition, did not affect occurrence, density or extinction. At the landscape scale, however, the species' occurrence was principally determined by the interactions among patch size, geographic isolation and landscape matrix. Isolation had the main independent contribution to explaining the probability of occurrence, followed by landscape matrix composition and patch size. The species' density was negatively correlated to patch size, suggesting crowding effects in small fragments, while extinction events were exclusively related to isolation. Our findings suggest that landscape rather than local population characteristics are crucial in determining the patterns of distribution and abundance of non-equilibrium populations in highly fragmented habitat networks. Consequently, conservation measures for these species should simultaneously involve patch size, isolation and landscape matrix and apply to the entire metapopulation rather than to particular patches.
Animals attacked by predators often enter a state of tonic immobility (TI) in which individuals a... more Animals attacked by predators often enter a state of tonic immobility (TI) in which individuals appear to simulate death. Despite the fact that TI is often used as a proxy of fear in domesticated animals, quantitative data on individual variation is very scarce for wild vertebrates. As a consequence, we lack ecological interpretations for the variability in TI that may exist in wild populations. Here, we tested whether there are consistent differences among individuals in 2 components of TI within wild populations of 2 avian species, the Yellow-crowned bishop (Euplectes afer) and the Tree sparrow (Passer montanus). We next tested whether this variation reflects variation in boldness toward predators (measured as the response to 2 predator models) or is simply related to variation in general activity/restlessness (measured as baseline activity) in the bishop. We analyzed our data by means of Bayesian structural equation modeling (SEM), which has several general advantages and, moreover, allowed us to analyze censored (truncated) data. We found good support for relatively high repeatability within individuals of both components of TI. Measures of TI appeared to be uncorrelated with baseline activity. In contrast, our results suggest that individual variation in TI in a wild vertebrate can be interpreted in a context of boldness toward predators, making TI a meaningful and practical behavioral trait for studies involving personality and antipredation behavior in wild populations. In addition, we show that the Bayesian structural equation modeling approach to analyze censored data had greater statistical power than other approaches. Hence, this rarely implemented technique deserves to be more widely used.
The moult of birds could greatly perturb the life cycle of feather mites (Astigmata). These mites... more The moult of birds could greatly perturb the life cycle of feather mites (Astigmata). These mites live on the surface of feathers and are unlikely to survive if they are on one when it is moulted. Therefore, we hypothesized that they would escape to other feathers to avoid this ...
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