Associations among MHC genes, latitude, and avian malaria infections in the rufous-collared sparrow (Zonotrichia capensis).

The major histocompatibility complex (MHC) is a genetic region in jawed vertebrates that contains key genes involved in the immune response. Associations between the MHC and avian malaria infections in wild birds have been observed and mainly explored in the Northern Hemisphere, while a general lack of information remains in the Southern Hemisphere. Here, we investigated the associations between the MHC genes and infections with Plasmodium and Haemoproteus blood parasites along a latitudinal gradient in South America. We sampled 93 rufous-collared sparrows (Zonotrichia capensis) individuals from four countries, Colombia, Ecuador, Peru, and Chile, and estimated MHC-I and MHC-II allele diversity. We detected between 1-4 (MHC-I) and 1-6 (MHC-II) amino acidic alleles per individual, with signs of positive selection. We obtained generalized additive mixed models to explore the associations between MHC-I and MHC-II diversity and latitude. We also explored the relationship between infection status and latitude/biome. We found a non-linear association between the MHC-II amino acidic allele diversity and latitude. Individuals from north Chile presented a lower MHC genetic diversity than those from other locations. We also found an association between deserts and xeric shrublands and a lower prevalence of Haemoproteus parasites. Our results support a lower MHC genetic in arid or semi-arid habitats in the region with the lower prevalence of Haemoproteus parasites.

The Complete Genome Sequences of 37 Bird Species from the Ecuadorian Andes.

We present the complete genome sequences of 37 Ecuadorian bird species widespread throughout the tropical Andes.

An elevational shift facilitated the Mesoamerican diversification of Azure-hooded Jays (Cyanolyca cucullata) during the Great American Biotic Interchange.

The Great American Biotic Interchange (GABI) was a key biogeographic event in the history of the Americas. The rising of the Panamanian land bridge ended the isolation of South America and ushered in a period of dispersal, mass extinction, and new community assemblages, which sparked competition, adaptation, and speciation. Diversification across many bird groups, and the elevational zonation of others, ties back to events triggered by the GABI. But the exact timing of these events is still being revealed, with recent studies suggesting a much earlier time window for faunal exchange, perhaps as early as 20 million years ago (Mya). Using a time-calibrated phylogenetic tree, we show that the jay genus Cyanolyca is emblematic of bird dispersal trends, with an early, pre-land bridge dispersal from Mesoamerica to South America 6.3-7.3 Mya, followed by a back-colonization of C. cucullata to Mesoamerica 2.3-4.8 Mya, likely after the land bridge was complete. As Cyanolyca species came into contact in Mesoamerica, they avoided competition due to a prior shift to lower elevation in the ancestor of C. cucullata. This shift allowed C. cucullata to integrate itself into the Mesoamerican highland avifauna, which our time-calibrated phylogeny suggests was already populated by higher-elevation, congeneric dwarf-jays (C. argentigula, C. pumilo, C. mirabilis, and C. nanus). The outcome of these events and fortuitous elevational zonation was that C. cucullata could continue colonizing new highland areas farther north during the Pleistocene. Resultingly, four C. cucullata lineages became isolated in allopatric, highland regions from Panama to Mexico, diverging in genetics, morphology, plumage, and vocalizations. At least two of these lineages are best described as species (C. mitrata and C. cucullata). Continued study will further document the influence of the GABI and help clarify how dispersal and vicariance shaped modern-day species assemblages in the Americas.

The performance of protected-area expansions in representing tropical Andean species: past trends and climate change prospects.

Protected area (PA) extent has increased significantly over the last 150 years globally, but it is yet unclear whether progress in expanding coverage has been accompanied by improved performance in ecological representation. Here, we explore temporal trends in the performance of PA networks in representing > 16,000 vertebrate and plant species in tropical Andean countries based on species bioclimatic niche modelling. We use a randomization analysis to assess whether representation gains over time (1937-2015) are the expected consequence of increasing the overall area of the network or the result of better designed networks. We also explore the impact of climate change on protected-area representation based on projected species distributions in 2070. We found that PAs added in the last three to four decades were better at representing species diversity than random additions overall. Threatened species, amphibians and reptiles are the exception. Species representation is projected to decrease across PAs under climate change, although PA expansions over the last decade (2006-2015) better represented species' future bioclimatic niches than did sites selected at random for most evaluated groups. These findings indicate an unbalanced representation across taxa, and raises concern over under-represented groups, including threatened species, and species' representation under climate change scenarios. However, they also suggest that decisions related to locating protected areas have become more strategic in recent decades and illustrate that indicators tracking representativeness of networks are crucial in PA monitoring frameworks.

Haemosporidian parasites in the ash-breasted Sierra finch (Geospizopsis plebejus): insights from an Andean dry forest population.

Haemosporidian genera Plasmodium, Haemoproteus and Leucocytozoon, responsible for avian malarial infections, are highly diverse and have a wide range of health effects and predictors, depending on the host and its environmental context. Here, we present, for the first time, detailed information on the identity, prevalence and parasitaemia of haemosporidians and other haemoparasites that infect the ash-breasted Sierra finch, Geospizopsis plebejus, in an Andean dry forest. We study the consequences of infection in the host body and health conditions and explore the environmental and intrinsic factors that influence infection status and parasitaemia. We conducted diagnoses by cytochrome b (cytb) sequencing and morphological identification, and estimated the levels of parasitaemia based on microscopy. We identified 6 cytb lineages infecting G. plebejus. Two of them were new lineages: Haemoproteus sp. GEPLE01 and GEPLE02. We also detected Haemoproteus sp. ZOCAP08, Haemoproteus sp. AMAVIR01, Plasmodium homopolare BAEBIC02 and Plasmodium cathemerium ZONCAP15. By microscopy, we detected Haemoproteus coatneyi, Haemoproteus erythrogravidus, P. homopolare and other unidentified species of Haemoproteus, Plasmodium, Babesia sp. and 1 microfilaria. We found no evidence of Leucocytozoon. Additionally, we detected several coinfections by sequencing and microscopy. The prevalence of haemosporidian infections was high (87.7%), and the mean parasitaemia was 61.65 infected cells per 10 000 erythrocytes examined. Prevalence and parasitaemia were higher for Haemoproteus than for Plasmodium. Haemoproteus sp. AMAVIR01 showed the highest prevalence (43.1%) and mean parasitaemia (94.39/10 000 erythrocytes) and might be associated with H. coatneyi. Immature individuals showed a lower prevalence than adults, supporting previous findings.

A set of principles and practical suggestions for equitable fieldwork in biology.

Field biology is an area of research that involves working directly with living organisms in situ through a practice known as "fieldwork." Conducting fieldwork often requires complex logistical planning within multiregional or multinational teams, interacting with local communities at field sites, and collaborative research led by one or a few of the core team members. However, existing power imbalances stemming from geopolitical history, discrimination, and professional position, among other factors, perpetuate inequities when conducting these research endeavors. After reflecting on our own research programs, we propose four general principles to guide equitable, inclusive, ethical, and safe practices in field biology: be collaborative, be respectful, be legal, and be safe. Although many biologists already structure their field programs around these principles or similar values, executing equitable research practices can prove challenging and requires careful consideration, especially by those in positions with relatively greater privilege. Based on experiences and input from a diverse group of global collaborators, we provide suggestions for action-oriented approaches to make field biology more equitable, with particular attention to how those with greater privilege can contribute. While we acknowledge that not all suggestions will be applicable to every institution or program, we hope that they will generate discussions and provide a baseline for training in proactive, equitable fieldwork practices.

Early stages of speciation with gene flow in the Amazilia Hummingbird (Amazilis amazilia) subspecies complex of Western South America.

Disentangling the factors underlying the diversification of geographically variable species with a wide geographical range is essential to understanding the initial stages and drivers of the speciation process. The Amazilia Hummingbird, Amazilis amazilia, is found along the Pacific coast from northern Ecuador down to the Nazca Valley of Peru, and is currently classified as six phenotypically differentiated subspecies. We aimed to resolve the evolutionary relationships of the six subspecies, to assess the geographical pattern and extent of evolutionary divergence, and to test for introgression using both a mtDNA marker and a genome-by-sequencing dataset from 86 individuals from across the species range. The consensus phylogenetic tree separated the six subspecies into three distinct clades, corresponding with the Ecuador lowlands (A. amazilia dumerilii), the Ecuador highlands (A. amazilia alticola and A. amazilia azuay), and the Peruvian coast (A. amazilia leucophoea, A. amazilia amazilia, and A. amazilia caeruleigularis). However, an unresolved mtDNA network suggests that the diversification of the subspecies was recent and rapid. We found evidence of gene flow among the subspecies A. amazilia dumerilii, A. amazilia alticola, and A. amazilia leucophoea, with strong genetic isolation of the subspecies A. amazilia azuay in the isolated Yunguilla Valley of Ecuador. Finally, environmental data from each subspecies' capture locations were concordant with the three distinct clades. Overall, our results suggest that both expansions into new habitats and geographic isolation shaped the present-day phylogeny and range of the A. amazilia subspecies, and that A. amazilia azuay may be genetically divergent enough to be considered a separate species.

A taxonomic assessment of Chlorospingus flavopectus phaeocephalus and Chlorospingus semifuscus (Passeriformes: Passerellidae), including the description of a new subspecies.

Chlorospingus flavopectus, a widely distributed member of the New World sparrows and finches (Passerellidae), is among the most variable and complex Neotropical bird species. With up to 28 subspecies that inhabit montane forest from Mexico south to Argentina, it presents a recurring leapfrog pattern, with many genetically differentiated lineages, but even more morphologically distinguishable taxa. Chlorospingus flavopectus phaeocephalus is distributed along the eastern Andean slope (from southern Colombia to northern Peru) and in localized patches along the central and southwestern slopes of the Ecuadorian Andes, in the forest remnants of Chimborazo, El Oro, and adjacent Loja provinces. This allopatric distribution was based on plumage similarities, but no genetic or vocal analysis has tested if these populations share a common ancestry. Here, we compared data for populations of C. f. phaeocephalus, C. semifuscus semifuscus from northwest Ecuador, and C. s. livingstoni from west Colombia, and analyzed them in the context of other Chlorospingus. Our phylogenetic analyses revealed that the putative west Ecuadorian populations of C. f. phaeocephalus are nested within C. semifuscus. They also present diagnostic characters when compared to other populations of C. semifuscus and C. f. phaeocephalus. Based on these results, we recognize the population from El Oro and adjacent Loja Provinces as a new subspecies of C. semifuscus, and the population from Chimborazo Province as a morphological variation of C. s. semifuscus.

International fisheries threaten globally endangered sharks in the Eastern Tropical Pacific Ocean: the case of the Fu Yuan Yu Leng 999 reefer vessel seized within the Galápagos Marine Reserve.

Shark fishing, driven by the fin trade, is the primary cause of global shark population declines. Here, we present a case study that exemplifies how industrial fisheries are likely depleting shark populations in the Eastern Tropical Pacific Ocean. In August 2017, the vessel Fu Yuan Yu Leng 999, of Chinese flag, was detained while crossing through the Galápagos Marine Reserve without authorization. This vessel contained 7639 sharks, representing one of the largest seizures recorded to date. Based on a sample of 929 individuals (12%), we found 12 shark species: 9 considered as Vulnerable or higher risk by the IUCN and 8 listed in CITES. Four species showed a higher proportion of immature than mature individuals, whereas size-distribution hints that at least some of the fishing ships associated with the operation may have been using purse-seine gear fishing equipment, which, for some species, goes against international conventions. Our data expose the magnitude of the threat that fishing industries and illegal trade represent to sharks in the Eastern Tropical Pacific Ocean.

The Expectations and Challenges of Wildlife Disease Research in the Era of Genomics: Forecasting with a Horizon Scan-like Exercise.

The outbreak and transmission of disease-causing pathogens are contributing to the unprecedented rate of biodiversity decline. Recent advances in genomics have coalesced into powerful tools to monitor, detect, and reconstruct the role of pathogens impacting wildlife populations. Wildlife researchers are thus uniquely positioned to merge ecological and evolutionary studies with genomic technologies to exploit unprecedented "Big Data" tools in disease research; however, many researchers lack the training and expertise required to use these computationally intensive methodologies. To address this disparity, the inaugural "Genomics of Disease in Wildlife" workshop assembled early to mid-career professionals with expertise across scientific disciplines (e.g., genomics, wildlife biology, veterinary sciences, and conservation management) for training in the application of genomic tools to wildlife disease research. A horizon scanning-like exercise, an activity to identify forthcoming trends and challenges, performed by the workshop participants identified and discussed 5 themes considered to be the most pressing to the application of genomics in wildlife disease research: 1) "Improving communication," 2) "Methodological and analytical advancements," 3) "Translation into practice," 4) "Integrating landscape ecology and genomics," and 5) "Emerging new questions." Wide-ranging solutions from the horizon scan were international in scope, itemized both deficiencies and strengths in wildlife genomic initiatives, promoted the use of genomic technologies to unite wildlife and human disease research, and advocated best practices for optimal use of genomic tools in wildlife disease projects. The results offer a glimpse of the potential revolution in human and wildlife disease research possible through multi-disciplinary collaborations at local, regional, and global scales.

Distributional patterns of Neotropical seasonally dry forest birds: a biogeographical regionalization.

Neotropical seasonally dry forests (NSDFs) are widely distributed and possess high levels of species richness and endemism; however, their biogeography remains only partially understood. Using species distribution modelling and parsimony analysis of endemicity, we analysed the distributional patterns of the NSDF avifauna in order to identify their areas of endemism and provide a better understanding of the historical relationships among those areas. The strict consensus trees revealed 17 areas of endemism for NSDFs, which involve four large regions: Baja California, Caribbean-Antilles islands, Mesoamerica and South America. These well-resolved clades are circumscribed by geographical and ecological barriers associated with the Gulf of California, the leading edge of the Caribbean plate, the Tehuantepec Isthmus, the Polochic-Motagua fault, the Nicaragua Depression, the Chocó forest, the Amazon basin and the Andean Cordillera. Relationships among groups of NSDFs found here suggest that evolution of their avifauna involved a mixture of vicariance and dispersal events. Our results support the idea of independent diversification patterns and biogeographical processes in each region, including those previously associated with the Pleistocene Arc Hypothesis for NSDFs of south-eastern South America. This study provides a biogeographical framework to open new lines of research related to the biotic diversification of NSDFs.

Avian haemosporidian infections in rufous-collared sparrows in an Andean dry forest: diversity and factors related to prevalence and parasitaemia.

Despite intensive research during the last few decades, understanding of ecological and physiological factors related to haemosporidian infections in birds is still fragmentary. Since more model organisms are needed in order to understand these infections in the wild, we analysed avian haemosporidian infections in the rufous-collared sparrow (Zonotrichia capensis, Emberizidae) in a dry forest of the Ecuadorian Andes. Parasite diversity was screened using molecular and morphological approaches. By molecular diagnosis, we identified three linages that were phylogenetically placed in the context of molecular haemosporidian diversity and associated with a morphospecies. By microscopy, we identified five described morphospecies and one additional undescribed morphospecies. We found that avian haemosporidian prevalence on the study site was 76.3%. Additionally, we used a series of generalized linear models to explore the potential relationship of parasite prevalence and parasitaemia with a set of variables related to physiological and environmental conditions. Although our results revealed associations of haemosporidian infections with precipitation, age and sampling site, the models only explained a small fraction of the variation.

Patterns of avian haemosporidian infections vary with time, but not habitat, in a fragmented Neotropical landscape.

Habitat loss has the potential to alter vertebrate host populations and their interactions with parasites. Theory predicts a decrease in parasite diversity due to the loss of hosts in such contexts. However, habitat loss could also increase parasite infections as a result of the arrival of new parasites or by decreasing host immune defenses. We investigated the effect of habitat loss and other habitat characteristics on avian haemosporidian infections in a community of birds within a fragmented landscape in northwest Ecuador. We estimated Plasmodium and Haemoproteus parasite infections in 504 individual birds belonging to 8 families and 18 species. We found differences in infection status among bird species, but no relationship between forest fragment characteristics and infection status was observed. We also found a temporal effect, with birds at the end of the five-month study (which ran from the end of the rainy season thru the dry season), being less infected by Plasmodium parasites than individuals sampled at the beginning. Moreover, we found a positive relationship between forest area and Culicoides abundance. Taken as a whole, these findings indicate little effect of fragment characteristics per se on infection, although additional sampling or higher infection rates would have offered more power to detect potential relationships.

Taxonomic Status of the Streaked Saltator, Saltator striatipectus (Passeriformes: Thraupidae), from Puná Island, Ecuador.

The Streaked Saltator, Saltator striatipectus, is an uncommon to common resident of open areas, cultivated land, gardens, and forest edges, with ten subspecies recognized from west Costa Rica through west Peru (Brewer 2016). Patterns of plumage variation, especially mantle color and streaking pattern below, are complex across subspecies and age classes (Chapman 1926; Ridgely Tudor 2009; Brewer 2016). Until recently, S. striatipectus was considered conspecific with the Lesser Antillean Saltator S. albicollis, but separated on the basis of genetic differentiation despite overall plumage similarities (Seutin et al. 1993). Actually, S. striatipectus and S. albicollis are not each other's closest relatives (Chaves et al. 2013).

On geographic barriers and Pleistocene glaciations: Tracing the diversification of the Russet-crowned Warbler (Myiothlypis coronata) along the Andes.

We studied the phylogeography and plumage variation of the Russet-crowned Warbler (Myiothlypis coronata), from Venezuela to Bolivia, with focus on populations from Ecuador and northern Peru. We analyzed sequences of mitochondrial and nuclear genes, geographic distributions, as well as photographs of specimens deposited at museum collections. Phylogenetic analyses identified three major lineages formed by populations from: Venezuela and Colombia (M. c. regulus), Ecuador and northern Peru (M. elata, M. castaneiceps, M. orientalis, M. c. chapmani), and central Peru and Bolivia (M. c. coronata). We found further population structure within M. c. regulus and M. c. coronata, and population structure and complexity of plumage variation within the Ecuador-northern Peru lineage. Time-calibrated trees estimated that most intraspecific variation originated during the Pleistocene; however, this pattern may not be attributed to an increase in diversification rate during that period. We discuss these results in the context of the importance of geographic-ecological barriers in promoting lineage diversification along the Andes and put forward a preliminary taxonomic proposal for major lineages identified in this study.

Complex coevolution of wing, tail, and vocal sounds of courting male bee hummingbirds.

Phenotypic characters with a complex physical basis may have a correspondingly complex evolutionary history. Males in the "bee" hummingbird clade court females with sound from tail-feathers, which flutter during display dives. On a phylogeny of 35 species, flutter sound frequency evolves as a gradual, continuous character on most branches. But on at least six internal branches fall two types of major, saltational changes: mode of flutter changes, or the feather that is the sound source changes, causing frequency to jump from one discrete value to another. In addition to their tail "instruments," males also court females with sound from their syrinx and wing feathers, and may transfer or switch instruments over evolutionary time. In support of this, we found a negative phylogenetic correlation between presence of wing trills and singing. We hypothesize this transference occurs because wing trills and vocal songs serve similar functions and are thus redundant. There are also three independent origins of self-convergence of multiple signals, in which the same species produces both a vocal (sung) frequency sweep, and a highly similar nonvocal sound. Moreover, production of vocal, learned song has been lost repeatedly. Male bee hummingbirds court females with a diverse, coevolving array of acoustic traits.

Large expansion of oil industry in the Ecuadorian Amazon: biodiversity vulnerability and conservation alternatives.

Ecuador will experience a significant expansion of the oil industry in its Amazonian region, one of the most biodiverse areas of the world. In view of the changes that are about to come, we explore the conflicts between oil extraction interests and biodiversity protection and apply systematic conservation planning to identify priority areas that should be protected in different oil exploitation scenarios. First, we quantified the current extent of oil blocks and protected zones and their overlap with two biodiversity indicators: 25 ecosystems and 745 species (whose distributions were estimated via species distribution models). With the new scheme of oil exploitation, oil blocks cover 68% (68,196 km(2)) of the Ecuadorian Amazon; half of it occupied by new blocks open for bids in the southern Amazon. This region is especially vulnerable to biodiversity losses, because peaks of species diversity, 19 ecosystems, and a third of its protected zones coincide spatially with oil blocks. Under these circumstances, we used Marxan software to identify priority areas for conservation outside oil blocks, but their coverage was insufficient to completely represent biodiversity. Instead, priority areas that include southern oil blocks provide a higher representation of biodiversity indicators. Therefore, preserving the southern Amazon becomes essential to improve the protection of Amazonian biodiversity in Ecuador, and avoiding oil exploitation in these areas (33% of the extent of southern oil blocks) should be considered a conservation alternative. Also, it is highly recommended to improve current oil exploitation technology to reduce environmental impacts in the region, especially within five oil blocks that we identified as most valuable for the conservation of biodiversity. The application of these and other recommendations depends heavily on the Ecuadorian government, which needs to find a better balance between the use of the Amazon resources and biodiversity conservation.

Testosterone and Haemosporidian Parasites Along a Tropical Elevational Gradient in Rufous-Collared Sparrows (Zonotrichia capensis).

Elevation has been proposed as a dominant ecological variable shaping life history traits and subsequently their underlying hormonal mechanisms. In an earlier meta-analysis of tropical birds, elevation was positively related to testosterone levels. Furthermore, parasitism by avian haemosporidians should vary with elevation as environmental conditions affect vector abundance, and while testosterone is needed for breeding, it is hypothesized to be immunosuppressive and thus could exacerbate haemosporidian infection. Our objective in this study was to examine the relationships between elevation, testosterone levels, and parasitism by avian haemosporidians. We surveyed breeding male rufous-collared sparrows (Zonotrichia capensis) across a wide elevational range along the equator. We measured baseline testosterone levels, haemosporidian infection at four elevations spanning the species' natural range in the Ecuadorian Andes (600, 1500, 2100, 3300 m). Testosterone levels from breeding males were not related to elevation, but there was high intrapopulation variability. Testosterone levels were not related to the probability of parasitism, but our results from one population suggested that the likelihood of being infected by haemosporidian parasites was greater when in breeding condition. In conclusion, even though there is variation in life history strategies among the studied populations, wider divergence in seasonality and life history traits would probably be needed to detect an effect of elevation on testosterone if one exists. Additionally, our results show that variation in testosterone is not related to infection risk of haemosporidians, thus other factors that take a toll on energetic resources, such as reproduction, should be looked at more closely.

Diurnal variation in corticosterone release among wild tropical forest birds.

BACKGROUND: Glucocorticoids are adrenal steroid hormones essential to homeostatic maintenance. Their daily variation at low concentrations regulates physiology and behavior to sustain proper immunological and metabolic function. Glucocorticoids rise well above these baseline levels during stress to elicit emergency-state responses that increase short-term survival. Despite this essence in managing life processes under both regular and adverse conditions, relationships of glucocorticoid release to environmental and intrinsic factors that vary at daily and seasonal scales are rarely studied in the wild. METHODS: This study on 41 passerine species of the Ecuadorian Chocó applied a standardized capture-and-restraint protocol to examine diurnal variation in baseline and stress-related release of corticosterone, the primary avian glucocorticoid. Tests for relationships to relative body mass, hemoglobin concentration, molt status and date complemented this evaluation of the time of day effect on corticosterone secretion in free-living tropical rainforest birds. Analyses were also partitioned by sex as well as performed separately on two common species, the wedge-billed woodcreeper and olive-striped flycatcher. RESULTS: Interspecific analyses indicated maximum baseline corticosterone levels at the onset of the active phase and reductions thereafter. Stress-related levels did not correspond to time of day but accompanied baseline reductions during molt and elevations in birds sampled later during the September - November study period. Baseline corticosterone related negatively to hemoglobin in the wedge-billed woodcreeper and stress-related levels increased with body mass in the olive-striped flycatcher. There were no substantial sex-related differences. CONCLUSIONS: The results of this study suggest a diurnal rhythmicity in baseline corticosterone release so robust as to emerge in pooled analyses across a highly variable dataset. While this detection in nature is singular, correspondent patterns have been demonstrated outside of the tropics in captive model species. Congruity in daily rhythms and links to physiological and life-history state across disparate taxa and environments may promote the yet unresolved utility of corticosterone release as a global metric for population health. However, certain results of this study also deviate from laboratory and field research at higher latitudes, cautioning generalization. Environmental distinctions such as high productivity and tempered seasonality may precipitate unique life-history strategies and underlying hormonal mechanisms in tropical rainforest birds.