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Fire regimes are a major agent of evolution in terrestrial animals. Changing fire regimes and the capacity for rapid evolution in wild animal populations suggests the potential for rapid, fire-driven adaptive animal evolution in the Pyrocene. Fire drives multiple modes of evolutionary change, including stabilizing, directional, disruptive, and fluctuating selection, and can strongly influence gene flow and genetic drift. Ongoing and future research in fire-driven animal evolution will benefit from further development of generalizable hypotheses, studies conducted in highly responsive taxa, and linking fire-adapted phenotypes to their underlying genetic basis. A better understanding of evolutionary responses to fire has the potential to positively influence conservation strategies that embrace evolutionary resilience to fire in the Pyrocene.
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AbstractThe extent to which species ranges reflect intrinsic physiological tolerances is a major question in evolutionary ecology. To date, consensus has been hindered by the limited tractability of experimental approaches across most of the tree of life. Here, we apply a macrophysiological approach to understand how hematological traits related to oxygen transport shape elevational ranges in a tropical biodiversity hot spot. Along Andean elevational gradients, we measured traits that affect blood oxygen-carrying capacity-total and cellular hemoglobin concentration and hematocrit, the volume percentage of red blood cells-for 2,355 individuals of 136 bird species. We used these data to evaluate the influence of hematological traits on elevational ranges. First, we asked whether the sensitivity of hematological traits to changes in elevation is predictive of elevational range breadth. Second, we asked whether variance in hematological traits changed as a function of distance to the nearest elevational range limit. We found that birds showing greater hematological sensitivity had broader elevational ranges, consistent with the idea that a greater acclimatization capacity facilitates elevational range expansion. We further found reduced variation in hematological traits in birds sampled near their elevational range limits and at high absolute elevations, patterns consistent with intensified natural selection, reduced effective population size, or compensatory changes in other cardiorespiratory traits. Our findings suggest that constraints on hematological sensitivity and local genetic adaptation to oxygen availability promote the evolution of the narrow elevational ranges that underpin tropical montane biodiversity.
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Biodiversidad , Aves , Humanos , Animales , Aves/fisiología , Fenotipo , Oxígeno , Ecología , AltitudRESUMEN
Predictable trait variation across environments suggests shared adaptive responses via repeated genetic evolution, phenotypic plasticity or both. Matching of trait-environment associations at phylogenetic and individual scales implies consistency between these processes. Alternatively, mismatch implies that evolutionary divergence has changed the rules of trait-environment covariation. Here we tested whether species adaptation alters elevational variation in blood traits. We measured blood for 1217 Andean hummingbirds of 77 species across a 4600-m elevational gradient. Unexpectedly, elevational variation in haemoglobin concentration ([Hb]) was scale independent, suggesting that physics of gas exchange, rather than species differences, determines responses to changing oxygen pressure. However, mechanisms of [Hb] adjustment did show signals of species adaptation: Species at either low or high elevations adjusted cell size, whereas species at mid-elevations adjusted cell number. This elevational variation in red blood cell number versus size suggests that genetic adaptation to high altitude has changed how these traits respond to shifts in oxygen availability.
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Altitud , Oxígeno , Animales , Filogenia , Aves/fisiología , FenotipoRESUMEN
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.
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Biodiversidad , Aves/genética , Genética de Población , Animales , Clima , Flujo Génico , Geografía , Nueva Guinea , Filogeografía , Polimorfismo Genético , Densidad de PoblaciónRESUMEN
Rapid species turnover in tropical mountains has fascinated biologists for centuries. A popular explanation for this heightened beta diversity is that climatic stability at low latitudes promotes the evolution of narrow thermal tolerance ranges, leading to local adaptation, evolutionary divergence and parapatric speciation along elevational gradients. However, an emerging consensus from research spanning phylogenetics, biogeography and behavioural ecology is that this process rarely, if ever, occurs. Instead, closely related species typically occupy a similar elevational niche, while species with divergent elevational niches tend to be more distantly related. These results suggest populations have responded to past environmental change not by adapting and diverging in place, but instead by shifting their distributions to tightly track climate over time. We argue that tropical species are likely to respond similarly to ongoing and future climate warming, an inference supported by evidence from recent range shifts. In the absence of widespread in situ adaptation to new climate regimes by tropical taxa, conservation planning should prioritize protecting large swaths of habitat to facilitate movement.
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Cambio Climático , Especiación Genética , Ecología , Ecosistema , FilogeniaRESUMEN
Genome-wide variation in introgression rates across hybrid zones offers a powerful opportunity for studying population differentiation. One poorly understood pattern of introgression is the geographic displacement of a trait implicated in lineage divergence from genome-wide population boundaries. While difficult to interpret, this pattern can facilitate the dissection of trait genetic architecture because traits become uncoupled from their ancestral genomic background. We studied an example of trait displacement generated by the introgression of head plumage coloration from personata to alba subspecies of the white wagtail. A previous study of their hybrid zone in Siberia revealed that the geographic transition in this sexual signal that mediates assortative mating was offset from other traits and genetic markers. Here we show that head plumage is associated with two small genetic regions. Despite having a simple genetic architecture, head plumage inheritance is consistent with partial dominance and epistasis, which could contribute to its asymmetric introgression.
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Introgresión Genética , Genoma , Passeriformes/genética , Pigmentación/genética , Carácter Cuantitativo Heredable , Animales , Quimera , Color , Epistasis Genética , Plumas/anatomía & histología , Plumas/metabolismo , Femenino , Masculino , Passeriformes/anatomía & histología , Passeriformes/clasificación , Siberia , UzbekistánRESUMEN
Closely related species with parapatric elevational ranges are ubiquitous in tropical mountains worldwide. The gradient speciation hypothesis proposes that these series are the result of in situ ecological speciation driven by divergent selection across elevation. Direct tests of this scenario have been hampered by the difficulty inferring the geographic arrangement of populations at the time of divergence. In cichlids, sticklebacks and Timema stick insects, support for ecological speciation driven by other selective pressures has come from demonstrating parallel speciation, where divergence proceeds independently across replicated environmental gradients. Here, we take advantage of the unique geography of the island of New Guinea to test for parallel gradient speciation in replicated populations of Syma kingfishers that show extremely subtle differentiation across elevation and between historically isolated mountain ranges. We find that currently described high-elevation and low-elevation species have reciprocally monophyletic gene trees and form nuclear DNA clusters, rejecting this hypothesis. However, demographic modelling suggests selection has likely maintained species boundaries in the face of gene flow following secondary contact. We compile evidence from the published literature to show that although in situ gradient speciation in labile organisms such as birds appears rare, divergent selection and post-speciation gene flow may be an underappreciated force in the origin of elevational series and tropical beta diversity along mountain slopes.
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Altitud , Aves/genética , Flujo Génico , Especiación Genética , Animales , Nueva Guinea , FilogeografíaRESUMEN
Janzen's seasonality hypothesis predicts that organisms inhabiting environments with limited climatic variability will evolve a reduced thermal tolerance breadth compared with organisms experiencing greater climatic variability. In turn, narrow tolerance breadth may select against dispersal across strong temperature gradients, such as those found across elevation. This can result in narrow elevational ranges and generate a pattern of isolation by environment or neutral genetic differentiation correlated with environmental variables that are independent of geographic distance. We tested for signatures of isolation by environment across elevation using genome-wide SNP data from five species of Andean dung beetles (subfamily Scarabaeinae) with well-characterized, narrow thermal physiologies, and narrow elevational distributions. Contrary to our expectations, we found no evidence of population genetic structure associated with elevation and little signal of isolation by environment. Further, elevational ranges for four of five species appear to be at equilibrium and show no decay of genetic diversity at range limits. Taken together, these results suggest physiological constraints on dispersal may primarily operate outside of a stable realized niche and point to a lower bound on the spatial scale of local adaptation.
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Incomplete or geographically biased sampling poses significant problems for research in phylogeography, population genetics, phylogenetics, and species delimitation. Despite the power of using genome-wide genetic markers in systematics and related fields, approaches such as the multispecies coalescent remain unable to easily account for unsampled lineages. The Empidonax difficilis/Empidonax occidentalis complex of small tyrannid flycatchers (Aves: Tyrannidae) is a classic example of widely distributed species with limited phenotypic geographic variation that was broken into two largely cryptic (or "sibling") lineages following extensive study. Though the group is well-characterized north of the US Mexico border, the evolutionary distinctiveness and phylogenetic relationships of southern populations remain obscure. In this article, we use dense genomic and geographic sampling across the majority of the range of the E. difficilis/E. occidentalis complex to assess whether current taxonomy and species limits reflect underlying evolutionary patterns, or whether they are an artifact of historically biased or incomplete sampling. We find that additional samples from Mexico render the widely recognized species-level lineage E. occidentalis paraphyletic, though it retains support in the best-fit species delimitation model from clustering analyses. We further identify a highly divergent unrecognized lineage in a previously unsampled portion of the group's range, which a cline analysis suggests is more reproductively isolated than the currently recognized species E. difficilis and E. occidentalis. Our phylogeny supports a southern origin of these taxa. Our results highlight the pervasive impacts of biased geographic sampling, even in well-studied vertebrate groups like birds, and illustrate what is a common problem when attempting to define species in the face of recent divergence and reticulate evolution.
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Marcadores Genéticos/genética , Filogenia , Pájaros Cantores/clasificación , Pájaros Cantores/genética , Animales , Variación Genética , México , Sesgo de Selección , Estados UnidosRESUMEN
A common method of minimizing errors in large DNA sequence data sets is to drop variable sites with a minor allele frequency (MAF) below some specified threshold. Although widespread, this procedure has the potential to alter downstream population genetic inferences and has received relatively little rigorous analysis. Here we use simulations and an empirical single nucleotide polymorphism data set to demonstrate the impacts of MAF thresholds on inference of population structure-often the first step in analysis of population genomic data. We find that model-based inference of population structure is confounded when singletons are included in the alignment, and that both model-based and multivariate analyses infer less distinct clusters when more stringent MAF cutoffs are applied. We propose that this behaviour is caused by the combination of a drop in the total size of the data matrix and by correlations between allele frequencies and mutational age. We recommend a set of best practices for applying MAF filters in studies seeking to describe population structure with genomic data.
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Biología Computacional/métodos , Frecuencia de los Genes , Genética de Población/métodos , Genómica/métodos , Animales , Simulación por Computador , Passeriformes/clasificación , Passeriformes/genética , Polimorfismo de Nucleótido SimpleRESUMEN
In the painted bunting (Passerina ciris), a North American songbird, populations on the Atlantic coast and interior southern United States are known to be allopatric during the breeding season, but efforts to map connectivity with wintering ranges have been largely inconclusive. Using genomic and morphological data from museum specimens and banded birds, we found evidence of three genetically differentiated painted bunting populations with distinct wintering ranges and molt-migration phenologies. In addition to confirming that the Atlantic coast population remains allopatric throughout the annual cycle, we identified an unexpected migratory divide within the interior breeding range. Populations breeding in Louisiana winter on the Yucatán Peninsula and are parapatric with other interior populations that winter in mainland Mexico and Central America. Across the interior breeding range, genetic ancestry is also associated with variation in wing length, suggesting that selection may be promoting morphological divergence in populations with different migration strategies.
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Migración Animal , Flujo Génico , Pájaros Cantores/genética , Animales , ADN Mitocondrial , Masculino , Filogeografía , Pájaros Cantores/anatomía & histología , Alas de Animales/anatomía & histologíaRESUMEN
Laboratory techniques for high-throughput sequencing have enhanced our ability to generate DNA sequence data from millions of natural history specimens collected prior to the molecular era, but remain poorly tested at shallower evolutionary time scales. Hybridization capture using restriction site-associated DNA probes (hyRAD) is a recently developed method for population genomics with museum specimens. The hyRAD method employs fragments produced in a restriction site-associated double digestion as the basis for probes that capture orthologous loci in samples of interest. While promising in that it does not require a reference genome, hyRAD has yet to be applied across study systems in independent laboratories. Here, we provide an independent assessment of the effectiveness of hyRAD on both fresh avian tissue and dried tissue from museum specimens up to 140 years old and investigate how variable quantities of input DNA affect sequencing, assembly, and population genetic inference. We present a modified bench protocol and bioinformatics pipeline, including three steps for detection and removal of microbial and mitochondrial DNA contaminants. We confirm that hyRAD is an effective tool for sampling thousands of orthologous SNPs from historic museum specimens to describe phylogeographic patterns. We find that modern DNA performs significantly better than historical DNA better during sequencing but that assembly performance is largely equivalent. We also find that the quantity of input DNA predicts %GC content of assembled contiguous sequences, suggesting PCR bias. We caution against sampling schemes that include taxonomic or geographic autocorrelation across modern and historic samples.
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Natural history museum collections (NHCs) represent a rich and largely untapped source of data on demography and population movements. NHC specimen records can be corrected to a crude measure of collecting effort and reflect relative population densities with a method known as abundance indices. We plotted abundance index values from georeferenced NHC data in a 12-month series for the new world migratory passerine Passerina ciris across its molting and wintering range in Mexico and Central America. We illustrated a statistically significant change in abundance index values across regions and months that suggests a quasi-circular movement around its non-breeding range, and used enhanced vegetation index (EVI) analysis of remote sensing plots to demonstrate non-random association of specimen record abundance with areas of high primary productivity. We demonstrated how abundance indices from NHC specimen records can be applied to infer previously unknown migratory behavior, and be integrated with remote sensing data to provide a deeper understanding of demography and behavioral ecology across time and space.
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"Supertramp" species are highly specialized overwater dispersers, and are useful taxa for investigating the influence of dispersal ability on speciation and diversification in island settings. The Louisiade White-eye (Zosterops griseotinctus) is a widespread avian supertramp endemic to Papua New Guinea's offshore islands. We used maximum likelihood and Bayesian inference to reconstruct phylogenetic relationships based on 2 mitochondrial and 1 nuclear loci (1813 bp total) from 88 individuals representing all 4 named subspecies and the full breadth of the species' range. We found significant geographic and population genetic structure, and support for a major clade containing the coral islets of the central Louisiade Archipelago and outlying Nissan Island. We found evidence of metapopulation structure and gene flow within the Louisiade Archipelago clade, and relatively high genetic distinctiveness of outlying island populations, including the population on volcanically-defaunated Long Island. We reject a hypothesis of panmixia within the Louisiade White-eye despite their long-range dispersal ability, and find evidence of selection against dispersal ability in populations on high-elevation islands where disturbance is rare. Our study represents a rare intraspecies phylogeny of an avian supertramp, and sheds light on patterns of evolution in highly vagile island species.