Multiple mutations in the Nav1.4 sodium channel of New Guinean toxic birds provide autoresistance to deadly batrachotoxin.

Toxicity has evolved multiple times across the tree of life and serves important functions related to hunting, defence and parasite deterrence. Toxins are produced either in situ by the toxic organism itself or associated symbionts, or acquired through diet. The ability to exploit toxins from external sources requires adaptations that prevent toxic effects on the consumer (autoresistance). Here, we examine genomic adaptations that could facilitate autoresistance to the diet-acquired potent neurotoxic alkaloid batrachotoxin (BTX) in New Guinean toxic birds. Our work documents two new toxic bird species and shows that toxic birds carry multiple mutations in the SCN4A gene that are under positive selection. This gene encodes the most common vertebrate muscle Nav channel (Nav1.4). Molecular docking results indicate that some of the mutations that are present in the pore-forming segment of the Nav channel, where BTX binds, could reduce its binding affinity. These mutations should therefore prevent the continuous opening of the sodium channels that BTX binding elicits, thereby preventing muscle paralysis and ultimately death. Although these mutations are different from those present in Neotropical Phyllobates poison dart frogs, they occur in the same segments of the Nav1.4 channel. Consequently, in addition to uncovering a greater diversity of toxic bird species than previously known, our work provides an intriguing example of molecular-level convergent adaptations allowing frogs and birds to ingest and use the same neurotoxin. This suggests that genetically modified Nav1.4 channels represent a key adaptation to BTX tolerance and exploitation across vertebrates.

Species-specific but not phylosymbiotic gut microbiomes of New Guinean passerine birds are shaped by diet and flight-associated gut modifications.

Animal hosts have evolved intricate associations with microbial symbionts, where both depend on each other for particular functions. In many cases, these associations lead to phylosymbiosis, where phylogenetically related species harbour compositionally more similar microbiomes than distantly related species. However, evidence for phylosymbiosis is either weak or lacking in gut microbiomes of flying vertebrates, particularly in birds. To shed more light on this phenomenon, we compared cloacal microbiomes of 37 tropical passerine bird species from New Guinea using 16S rRNA bacterial gene sequencing. We show a lack of phylosymbiosis and document highly variable microbiomes. Furthermore, we find that gut bacterial community compositions are species-specific and tend to be shaped by host diet but not sampling locality, potentially driven by the similarities in habitats used by individual species. We further show that flight-associated gut modifications, coupled with individual dietary differences, shape gut microbiome structure and variation, contributing to the lack of phylosymbiosis. These patterns indicate that the stability of symbiosis may depend on microbial functional diversity rather than taxonomic composition. Furthermore, the more variable and fluid host-microbe associations suggest probable disparities in the potential for coevolution between bird host species and microbial symbionts.

Last Glacial Maximum led to community-wide population expansion in a montane songbird radiation in highland Papua New Guinea.

BACKGROUND: Quaternary climate fluctuations are an engine of biotic diversification. Global cooling cycles, such as the Last Glacial Maximum (LGM), are known to have fragmented the ranges of higher-latitude fauna and flora into smaller refugia, dramatically reducing species ranges. However, relatively less is known about the effects of cooling cycles on tropical biota. RESULTS: We analyzed thousands of genome-wide DNA markers across an assemblage of three closely related understorey-inhabiting scrubwrens (Sericornis and Aethomyias; Aves) from montane forest along an elevational gradient on Mt. Wilhelm, the highest mountain of Papua New Guinea. Despite species-specific differences in elevational preference, we found limited differentiation within each scrubwren species, but detected a strong genomic signature of simultaneous population expansions at 27-29 ka, coinciding with the onset of the LGM. CONCLUSION: The remarkable synchronous timing of population expansions of all three species demonstrates the importance of global cooling cycles in expanding highland habitat. Global cooling cycles have likely had strongly different impacts on tropical montane areas versus boreal and temperate latitudes, leading to population expansions in the former and serious fragmentation in the latter.

Spatiotemporal patterns of avian host-parasite interactions in the face of biogeographical range expansions.

Exploration of interactions between hosts and parasitic symbionts is important for our understanding of the temporal and spatial distribution of organisms. For example, host colonization of new geographical regions may alter levels of infections and parasite specificity, and even allow hosts to escape from co-evolved parasites, consequently shaping spatial distributions and community structure of both host and parasite. Here we investigate the effect of host colonization of new regions and the elevational distribution of host-parasite associations between birds and their vector-transmitted haemosporidian blood parasites in two geological and geographical settings: mountains of New Guinea and the Canary Islands. Our results demonstrate that bird communities in younger regions have significantly lower levels of parasitism compared to those of older regions. Furthermore, host-parasite network analyses demonstrate that blood parasites may respond differently after arriving to a new region, through adaptations that allow for either expanding (Canary Islands) or retaining (New Guinea) their host niches. The spatial prevalence patterns along elevational gradients differed in the two regions, suggesting that region-specific biotic (e.g., host community) and abiotic factors (e.g., temperature) govern prevalence patterns. Our findings suggest that the spatiotemporal range dynamics in host-parasite systems are driven by multiple factors, but that host and parasite community compositions and colonization histories are of particular importance.

Reorganization of bird communities along a rainforest elevation gradient during a strong El Niño event in Papua New Guinea.

The El Niño 2015 event, most extreme since 1997, led to severe droughts in tropical wet Papua New Guinea (PNG), reducing May to October dry season rainfall by 75% in the lowlands and 25% in the highlands. Such droughts are likely to have significant effects on terrestrial ecosystems, but they have been poorly explored in Papua New Guinea. Here, we report changes in bird community composition prior to, during, and after the 2015 El Niño event along the elevational gradient ranging from 200 m to 2700 m a.s.l. at the Mt. Wilhelm rainforest in PNG. The abundance of birds in the lowlands dropped by 60% but increased by 40% at elevations above 1700 m during El Niño year. In the following year, the individual bird species reached mean population sizes similar to pre-El Niño years but did not fully recover. Species richness roughly followed the pattern of observed abundance and quickly and fully re-established after the event to the pre- El Niño values. Thus, at least some terrestrial birds seem to react quickly to the extreme droughts in lowlands and shift to less affected mountain habitats. We recorded upper elevational range limits to shifts by more than 500 m a.s.l. in 22 bird species (out of 237 recorded in total) during El Niño year, in contrast to their typical ranges. Our study suggests that a strong El Niño event can have strong but reversible effects on bird communities as long as they have an opportunity to move to more favorable sites through undisturbed habitats.

Population genomics of the island thrush elucidates one of earth's great archipelagic radiations.

Tropical islands are renowned as natural laboratories for evolutionary study. Lineage radiations across tropical archipelagos are ideal systems for investigating how colonization, speciation, and extinction processes shape biodiversity patterns. The expansion of the island thrush across the Indo-Pacific represents one of the largest yet most perplexing island radiations of any songbird species. The island thrush exhibits a complex mosaic of pronounced plumage variation across its range and is arguably the world's most polytypic bird. It is a sedentary species largely restricted to mountain forests, yet it has colonized a vast island region spanning a quarter of the globe. We conducted a comprehensive sampling of island thrush populations and obtained genome-wide SNP data, which we used to reconstruct its phylogeny, population structure, gene flow, and demographic history. The island thrush evolved from migratory Palearctic ancestors and radiated explosively across the Indo-Pacific during the Pleistocene, with numerous instances of gene flow between populations. Its bewildering plumage variation masks a biogeographically intuitive stepping stone colonization path from the Philippines through the Greater Sundas, Wallacea, and New Guinea to Polynesia. The island thrush's success in colonizing Indo-Pacific mountains can be understood in light of its ancestral mobility and adaptation to cool climates; however, shifts in elevational range, degree of plumage variation and apparent dispersal rates in the eastern part of its range raise further intriguing questions about its biology.

Specific gut bacterial responses to natural diets of tropical birds.

The composition of gut bacterial communities is strongly influenced by the host diet in many animal taxa. For birds, the effect of diet on the microbiomes has been documented through diet manipulation studies. However, for wild birds, most studies have drawn on literature-based information to decipher the dietary effects, thereby, overlooking individual variation in dietary intake. Here we examine how naturally consumed diets influence the composition of the crop and cloacal microbiomes of twenty-one tropical bird species, using visual and metabarcoding-based identification of consumed diets and bacterial 16S rRNA microbiome sequencing. We show that diet intakes vary markedly between individuals of the same species and that literature-based dietary guilds grossly underestimate intraspecific diet variability. Furthermore, despite an effect of literature-based dietary guild assignment of host taxa, the composition of natural diets does not align with crop and cloacal microbiome similarity. However, host-taxon specific gut bacterial lineages are positively correlated with specific diet items, indicating that certain microbes associate with different diet components in specific avian hosts. Consequently, microbiome composition is not congruent with the overall consumed diet composition of species, but specific components of a consumed diet lead to host-specific effects on gut bacterial taxa.

The formation of avian montane diversity across barriers and along elevational gradients.

Tropical mountains harbor exceptional concentrations of Earth's biodiversity. In topographically complex landscapes, montane species typically inhabit multiple mountainous regions, but are absent in intervening lowland environments. Here we report a comparative analysis of genome-wide DNA polymorphism data for population pairs from eighteen Indo-Pacific bird species from the Moluccan islands of Buru and Seram and from across the island of New Guinea. We test how barrier strength and relative elevational distribution predict population differentiation, rates of historical gene flow, and changes in effective population sizes through time. We find population differentiation to be consistently and positively correlated with barrier strength and a species' altitudinal floor. Additionally, we find that Pleistocene climate oscillations have had a dramatic influence on the demographics of all species but were most pronounced in regions of smaller geographic area. Surprisingly, even the most divergent taxon pairs at the highest elevations experience gene flow across barriers, implying that dispersal between montane regions is important for the formation of montane assemblages.

Biomass, abundances, and abundance and geographical range size relationship of birds along a rainforest elevational gradient in Papua New Guinea.

The usually positive inter-specific relationship between geographical range size and the abundance of local bird populations comes with exceptions. On continents, the majority of these exceptions have been described from tropical montane areas in Africa, where geographically-restricted bird species are unusually abundant. We asked how the local abundances of passerine and non-passerine bird species along an elevational gradient on Mt. Wilhelm, Papua New Guinea relate to their geographical range size. We collected data on bird assemblages at eight elevations (200-3,700 m, at 500 m elevational increments). We used a standardized point-counts at 16 points at each elevational study site. We partitioned the birds into feeding guilds, and we obtained data on geographical range sizes from the Bird-Life International data zone. We observed a positive relationship between abundance and geographical range size in the lowlands. This trend changed to a negative one towards higher elevations. The total abundances of the assemblage showed a hump-shaped pattern along the elevational gradient, with passerine birds, namely passerine insectivores, driving the observed pattern. In contrast to abundances, the mean biomass of the bird assemblages decreased with increasing elevation. Our results show that montane bird species maintain dense populations which compensate for the decreased available area near the top of the mountain.

Gene Flow in the Müllerian Mimicry Ring of a Poisonous Papuan Songbird Clade (Pitohui; Aves).

Müllerian mimicry rings are remarkable symbiotic species assemblages in which multiple members share a similar phenotype. However, their evolutionary origin remains poorly understood. Although gene flow among species has been shown to generate mimetic patterns in some Heliconius butterflies, mimicry is believed to be due to true convergence without gene flow in many other cases. We investigated the evolutionary history of multiple members of a passerine mimicry ring in the poisonous Papuan pitohuis. Previous phylogenetic evidence indicates that the aposematic coloration shared by many, but not all, members of this genus is ancestral and has only been retained by members of the mimicry ring. Using a newly assembled genome and thousands of genomic DNA markers, we demonstrate gene flow from the hooded pitohui (Pitohui dichrous) into the southern variable pitohui (Pitohui uropygialis), consistent with shared patterns of aposematic coloration. The vicinity of putatively introgressed loci is significantly enriched for genes that are important in melanin pigment expression and toxin resistance, suggesting that gene flow may have been instrumental in the sharing of plumage patterns and toxicity. These results indicate that interspecies gene flow may be a more general mechanism in generating mimicry rings than hitherto appreciated.

Diet of land birds along an elevational gradient in Papua New Guinea.

Food preferences and exploitation are crucial to many aspects of avian ecology and are of increasing importance as we progress in our understanding of community ecology. We studied birds and their feeding specialization in the Central Range of Papua New Guinea, at eight study sites along a complete (200 to 3700 m a.s.l.) rainforest elevational gradient. The relative species richness and abundance increased with increasing elevation for insect and nectar eating birds, and decreased with elevation for fruit feeding birds. Using emetic tartar, we coerced 999 individuals from 99 bird species to regurgitate their stomach contents and studied these food samples. The proportion of arthropods in food samples increased with increasing elevation at the expense of plant material. Body size of arthropods eaten by birds decreased with increasing elevation. This reflected the parallel elevational trend in the body size of arthropods available in the forest understory. Body size of insectivorous birds was significantly positively correlated with the body size of arthropods they ate. Coleoptera were the most exploited arthropods, followed by Araneae, Hymenoptera, and Lepidoptera. Selectivity indexes showed that most of the arthropod taxa were taken opportunistically, reflecting the spatial patterns in arthropod abundances to which the birds were exposed.

Higher predation risk for insect prey at low latitudes and elevations.

Biotic interactions underlie ecosystem structure and function, but predicting interaction outcomes is difficult. We tested the hypothesis that biotic interaction strength increases toward the equator, using a global experiment with model caterpillars to measure predation risk. Across an 11,660-kilometer latitudinal gradient spanning six continents, we found increasing predation toward the equator, with a parallel pattern of increasing predation toward lower elevations. Patterns across both latitude and elevation were driven by arthropod predators, with no systematic trend in attack rates by birds or mammals. These matching gradients at global and regional scales suggest consistent drivers of biotic interaction strength, a finding that needs to be integrated into general theories of herbivory, community organization, and life-history evolution.