RESUMO
High-altitude environments require that animals meet the metabolic O2 demands for locomotion and thermogenesis in O2-thin air, but the degree to which convergent metabolic changes have arisen across independent high-altitude lineages or the speed at which such changes arise is unclear. We examined seven high-altitude waterfowl that have inhabited the Andes (3812-4806 m elevation) over varying evolutionary time scales, to elucidate changes in biochemical pathways of energy metabolism in flight muscle relative to low-altitude sister taxa. Convergent changes across high-altitude taxa included increased hydroxyacyl-coA dehydrogenase and succinate dehydrogenase activities, decreased lactate dehydrogenase, pyruvate kinase, creatine kinase, and cytochrome c oxidase activities, and increased myoglobin content. ATP synthase activity increased in only the longest established high-altitude taxa, whereas hexokinase activity increased in only newly established taxa. Therefore, changes in pathways of lipid oxidation, glycolysis, and mitochondrial oxidative phosphorylation are common strategies to cope with high-altitude hypoxia, but some changes require longer evolutionary time to arise.
Assuntos
Anseriformes/metabolismo , Evolução Biológica , Metabolismo Energético , Músculo Esquelético/metabolismo , Altitude , Distribuição Animal , Animais , América do SulRESUMO
The cardiovascular system is critical for delivering O2 to tissues. Here, we examined the cardiovascular responses to progressive hypoxia in four high-altitude Andean duck species compared with four related low-altitude populations in North America, tested at their native altitude. Ducks were exposed to stepwise decreases in inspired partial pressure of O2 while we monitored heart rate, O2 consumption rate, blood O2 saturation, haematocrit (Hct) and blood haemoglobin (Hb) concentration. We calculated O2 pulse (the product of stroke volume and the arterial-venous O2 content difference), blood O2 concentration and heart rate variability. Regardless of altitude, all eight populations maintained O2 consumption rate with minimal change in heart rate or O2 pulse, indicating that O2 consumption was maintained by either a constant arterial-venous O2 content difference (an increase in the relative O2 extracted from arterial blood) or by a combination of changes in stroke volume and the arterial-venous O2 content difference. Three high-altitude taxa (yellow-billed pintails, cinnamon teal and speckled teal) had higher Hct and Hb concentration, increasing the O2 content of arterial blood, and potentially providing a greater reserve for enhancing O2 delivery during hypoxia. Hct and Hb concentration between low- and high-altitude populations of ruddy duck were similar, representing a potential adaptation to diving life. Heart rate variability was generally lower in high-altitude ducks, concurrent with similar or lower heart rates than low-altitude ducks, suggesting a reduction in vagal and sympathetic tone. These unique features of the Andean ducks differ from previous observations in both Andean geese and bar-headed geese, neither of which exhibit significant elevations in Hct or Hb concentration compared with their low-altitude relatives, revealing yet another avian strategy for coping with high altitude.
Assuntos
Adaptação Biológica , Altitude , Patos/fisiologia , Consumo de Oxigênio , Anaerobiose , Animais , Animais Selvagens/fisiologia , América do Norte , PeruRESUMO
We examined the control of breathing and respiratory gas exchange in six species of high-altitude duck that independently colonized the high Andes. We compared ducks from high-altitude populations in Peru (Lake Titicaca at â¼3800â m above sea level; Chancay River at â¼3000-4100â m) with closely related populations or species from low altitude. Hypoxic ventilatory responses were measured shortly after capture at the native altitude. In general, ducks responded to acute hypoxia with robust increases in total ventilation and pulmonary O2 extraction. O2 consumption rates were maintained or increased slightly in acute hypoxia, despite â¼1-2°C reductions in body temperature in most species. Two high-altitude taxa - yellow-billed pintail and torrent duck - exhibited higher total ventilation than their low-altitude counterparts, and yellow-billed pintail exhibited greater increases in pulmonary O2 extraction in severe hypoxia. In contrast, three other high-altitude taxa - Andean ruddy duck, Andean cinnamon teal and speckled teal - had similar or slightly reduced total ventilation and pulmonary O2 extraction compared with low-altitude relatives. Arterial O2 saturation (SaO2 ) was elevated in yellow-billed pintails at moderate levels of hypoxia, but there were no differences in SaO2 in other high-altitude taxa compared with their close relatives. This finding suggests that improvements in SaO2 in hypoxia can require increases in both breathing and haemoglobin-O2 affinity, because the yellow-billed pintail was the only high-altitude duck with concurrent increases in both traits compared with its low-altitude relative. Overall, our results suggest that distinct physiological strategies for coping with hypoxia can exist across different high-altitude lineages, even among those inhabiting very similar high-altitude habitats.
Assuntos
Aclimatação , Altitude , Temperatura Corporal/fisiologia , Patos/fisiologia , Animais , Feminino , Hipóxia , Masculino , Oregon , Consumo de Oxigênio/fisiologia , Peru , RespiraçãoRESUMO
During periods of reduced O2 supply, the most profound changes in gene expression are mediated by hypoxia-inducible factor (HIF) transcription factors that play a key role in cellular responses to low-O2 tension. Using target-enrichment sequencing, we tested whether variation in 26 genes in the HIF signaling pathway was associated with high altitude and therefore corresponding O2 availability in three duck species that colonized the Andes from ancestral low-altitude habitats in South America. We found strong support for convergent evolution in the case of two of the three duck species with the same genes (EGLN1, EPAS1), and even the same exons (exon 12, EPAS1), exhibiting extreme outliers with a high probability of directional selection in the high-altitude populations. These results mirror patterns of adaptation seen in human populations, which showed mutations in EPAS1, and transcriptional regulation differences in EGLN1, causing changes in downstream target transactivation, associated with a blunted hypoxic response.
Assuntos
Fatores de Transcrição Hélice-Alça-Hélice Básicos/genética , Patos/genética , Prolina Dioxigenases do Fator Induzível por Hipóxia/genética , Aclimatação , Adaptação Fisiológica , Altitude , Animais , Fatores de Transcrição Hélice-Alça-Hélice Básicos/metabolismo , Patos/metabolismo , Éxons , Humanos , Prolina Dioxigenases do Fator Induzível por Hipóxia/metabolismo , Oxigênio/metabolismo , Seleção Genética , América do SulRESUMO
High-altitude bar-headed geese (Anser indicus) and Andean geese (Chloephaga melanoptera) have been shown to preferentially increase tidal volume over breathing frequency when increasing ventilation during exposure to hypoxia. Increasing tidal volume is a more effective breathing strategy but is also thought to be more mechanically and metabolically expensive. We asked whether there might be differences in the mechanics or morphology of the respiratory systems of high-altitude transient bar-headed geese and high-altitude resident Andean geese that could minimize the cost of breathing more deeply. We compared these two species with a low-altitude migratory species, the barnacle goose (Branta leucopsis). We ventilated anesthetized birds to measure mechanical properties of the respiratory system and used CT scans to quantify respiratory morphology. We found that the respiratory system of Andean geese was disproportionately larger than that of the other two species, allowing use of a deeper breathing strategy for the same energetic cost. The relative size of the respiratory system, especially the caudal air sacs, of bar-headed geese was also larger than that of barnacle geese. However, when normalized to respiratory system size, the mechanical cost of breathing did not differ significantly among these three species, indicating that deeper breathing is enabled by morphological but not mechanical differences between species. The metabolic cost of breathing was estimated to be <1% of basal metabolic rate at rest in normoxia. Because of differences in the magnitude of the ventilatory response, the cost of breathing was estimated to increase 7- to 10-fold in bar-headed and barnacle geese in severe hypoxia, but less than 1-fold in Andean geese exposed to the same low atmospheric PO2.
Assuntos
Migração Animal , Gansos/anatomia & histologia , Gansos/fisiologia , Mecânica Respiratória , Sistema Respiratório/anatomia & histologia , Altitude , Animais , Feminino , Voo Animal , Pulmão/anatomia & histologia , Pulmão/fisiologia , Masculino , América do Sul , Especificidade da Espécie , Tibet , Volume de Ventilação PulmonarRESUMO
Torrent ducks inhabit fast-flowing rivers in the Andes from sea level to altitudes up to 4500â m. We examined the mitochondrial physiology that facilitates performance over this altitudinal cline by comparing the respiratory capacities of permeabilized fibers, the activities of 16 key metabolic enzymes and the myoglobin content in muscles between high- and low-altitude populations of this species. Mitochondrial respiratory capacities (assessed using substrates of mitochondrial complexes I, II and/or IV) were higher in highland ducks in the gastrocnemius muscle - the primary muscle used to support swimming and diving - but were similar between populations in the pectoralis muscle and the left ventricle. The heightened respiratory capacity in the gastrocnemius of highland ducks was associated with elevated activities of cytochrome oxidase, phosphofructokinase, pyruvate kinase and malate dehydrogenase (MDH). Although respiratory capacities were similar between populations in the other muscles, highland ducks had elevated activities of ATP synthase, lactate dehydrogenase, MDH, hydroxyacyl CoA dehydrogenase and creatine kinase in the left ventricle, and elevated MDH activity and myoglobin content in the pectoralis. Thus, although there was a significant increase in the oxidative capacity of the gastrocnemius in highland ducks, which correlates with improved performance at high altitudes, the variation in metabolic enzyme activities in other muscles not correlated to respiratory capacity, such as the consistent upregulation of MDH activity, may serve other functions that contribute to success at high altitudes.
Assuntos
Altitude , Patos/fisiologia , Metabolismo Energético/fisiologia , Mitocôndrias/metabolismo , Músculo Esquelético/metabolismo , Miocárdio/metabolismo , Músculos Peitorais/metabolismo , Acetil-CoA C-Acetiltransferase/metabolismo , Migração Animal/fisiologia , Animais , Creatina Quinase/metabolismo , Complexo IV da Cadeia de Transporte de Elétrons/metabolismo , Ventrículos do Coração/metabolismo , Lactato Desidrogenases/metabolismo , Malato Desidrogenase/metabolismo , Mitocôndrias/fisiologia , Mioglobina/metabolismo , Fosfofrutoquinases/metabolismo , Piruvato Quinase/metabolismo , América do SulRESUMO
Spatial variation in the environment can lead to divergent selection between populations occupying different parts of a species' range, and ultimately lead to population divergence. The colonization of new areas can thus facilitate divergence in beneficial traits, yet with little differentiation at neutral genetic markers. We investigated genetic and phenotypic patterns of divergence between low- and high-altitude populations of cinnamon teal inhabiting normoxic and hypoxic regions in the Andes and adjacent lowlands of South America. Cinnamon teal showed strong divergence in body size (PC1; P(ST) = 0.56) and exhibited significant frequency differences in a single nonsynonymous α-hemoglobin amino acid polymorphism (Asn/Ser-α9; F(ST) = 0.60) between environmental extremes, despite considerable admixture of mtDNA and intron loci (F(ST) = 0.004-0.168). Inferences of strong population segregation were further supported by the observation of few mismatched individuals in either environmental extreme. Coalescent analyses indicated that the highlands were most likely colonized from lowland regions but following divergence, gene flow has been asymmetric from the highlands into the lowlands. Multiple selection pressures associated with high-altitude habitats, including cold and hypoxia, have likely shaped morphological and genetic divergence within South American cinnamon teal populations.
Assuntos
Patos/genética , Ecossistema , Evolução Molecular , Especiação Genética , Genótipo , Fenótipo , Ar , Altitude , Animais , Tamanho Corporal/genética , Temperatura Baixa , DNA Mitocondrial/genética , Variação Genética , Hemoglobinas/genética , Íntrons , Oxigênio , População/genética , América do SulRESUMO
Interspecific hybridization is common in plants and animals, particularly in waterfowl (Anatidae). One factor shown to contribute to hybridization is restricted mate choice, which can occur when two species occur in sympatry but one is rare. The Hubbs principle, or "desperation hypothesis," states that under such circumstances the rarer species is more likely to mate with heterospecifics. Here we report interspecific hybridization between two waterfowl species that coexist in broad sympatry and mixed flocks throughout southern South America. Speckled teal (Anas flavirostris) and yellow-billed pintails (Anas georgica) are abundant in continental South America, but in the Falkland Islands speckled teal outnumber yellow-billed pintails approximately ten to one. Using eight genetic loci (mtDNA and 7 nuclear introns) coupled with Bayesian assignment tests and relatedness analysis, we identified a speckled teal x yellow-billed pintail F(1) hybrid female and her duckling sired by a male speckled teal. Although our sample in the Falkland Islands was small, we failed to identify unequivocal evidence of hybridization or introgression in a much larger sample from Argentina using a three-population "isolation with migration" coalescent analysis. While additional data are needed to determine if this event in the Falkland Islands was a rare singular occurrence, our results provide further support for the "desperation hypothesis," which states that scarcity in one population and abundance of another will often lead to hybridization.
Assuntos
Patos/genética , Fluxo Gênico/genética , Hibridização Genética , Alelos , Animais , Argentina , Núcleo Celular/genética , Galinhas/genética , Cromossomos/genética , Cruzamentos Genéticos , Ilhas Malvinas , Feminino , Redes Reguladoras de Genes/genética , Loci Gênicos/genética , Variação Genética , Genoma/genética , Geografia , Masculino , Dinâmica Populacional , Especificidade da EspécieRESUMO
Hypoxia is one of the most important factors affecting survival at high altitude, and the major hemoglobin protein is a likely target of selection. We compared population genetic structure in the alphaA and betaA hemoglobin subunits (HBA2 and HBB) of five paired lowland and highland populations of Andean dabbling ducks to unlinked reference loci. In the hemoglobin genes, parallel amino acid replacements were overrepresented in highland lineages, and one to five derived substitutions occurred at external solvent-accessible positions on the alpha and beta subunits, at alpha(1)beta(1) intersubunit contacts, or in close proximity to inositolpentaphosphate (IPP) binding sites. Coalescent analyses incorporating the stochasticity of drift and mutation indicated that hemoglobin alleles were less likely to be transferred between highland and lowland populations than unlinked alleles at five other loci. Amino acid replacements that were overrepresented in the highlands were rarely found within lowland populations, suggesting that alleles segregating at high frequency in the highlands may be maladaptive in the lowlands and vice versa. Most highland populations are probably nonmigratory and locally adapted to the Altiplano, but gene flow for several species may be sufficiently high to retard divergence at unlinked loci. Heterozygosity was elevated in the alphaA or betaA subunits of highland populations exhibiting high gene flow between the southern lowlands and the highlands and in highland species that disperse seasonally downslope to midelevation environments from the central Andean plateau. However, elevated heterozygosity occurred more frequently in the alphaA subunit but not simultaneously in both subunits, suggesting that selection may be more constrained by epistasis in the betaA subunit. Concordant patterns among multiple species with different evolutionary histories and depths of historical divergence and gene flow suggest that the major hemoglobin genes of these five dabbling duck species have evolved adaptively in response to high-altitude hypoxia in the Andes.
Assuntos
Adaptação Biológica/genética , Altitude , Patos/genética , Evolução Molecular , alfa-Globinas/genética , Globinas beta/genética , Substituição de Aminoácidos , Migração Animal , Animais , Patos/fisiologia , Frequência do Gene , Genótipo , Polimorfismo Genético , Dinâmica Populacional , Análise de Sequência de DNA , Análise de Sequência de Proteína , América do SulRESUMO
When populations become locally adapted to contrasting environments, alleles that have high fitness in only one environment may be quickly eliminated in populations adapted to other environments, such that gene flow is partly restricted. The stronger the selection, the more rapidly immigrant alleles of lower fitness will be eliminated from the population. However, gene flow may continue to occur at unlinked loci, and adaptive divergence can proceed in the face of countervailing gene flow if selection is strong relative to migration (s > m). We studied the population genetics of the major hemoglobin genes in yellow-billed pintails (Anas georgica) experiencing contrasting partial pressures of oxygen in the Andes of South America. High gene flow and weak population subdivision were evident at seven putatively neutral loci in different chromosomal linkage groups. In contrast, amino acid replacements (Ser-beta13, Ser-beta116, and Met-beta133) in the betaA hemoglobin subunit segregated by elevation between lowland and highland populations with significantly elevated F(ST). Migration rates for the betaA subunit alleles were approximately 17-24 times smaller than for five unlinked reference loci, the alphaA hemoglobin subunit (which lacks amino acid replacements) and the mitochondrial DNA control region. The betaA subunit alleles of yellow-billed pintails were half as likely to be transferred downslope, from the highlands to the lowlands, than in the opposite direction upslope. We hypothesize that migration between the lowlands and highlands is restricted by local adaptation, and the betaA hemoglobin subunit is a likely target of selection related to high-altitude hypoxia; however, gene flow may be sufficiently high to retard divergence at most unlinked loci. Individuals homozygous for lowland alleles may have relatively little difficulty dispersing to the highlands initially but may experience long-term fitness reduction. Individuals homozygous for highland genotypes, in contrast, would be predicted to have difficulty dispersing to the lowlands if their hemoglobin alleles confer high oxygen affinity, predicted to result in chronic erythrocytosis at low elevation. Heterozygous individuals may have a dispersal advantage if their hemoglobin has a wider range of function due to the presence of multiple protein isoforms with a mixture of different oxygen affinities.
Assuntos
Patos/genética , Fluxo Gênico , Seleção Genética , Globinas beta/genética , Globinas beta/metabolismo , Animais , Patos/metabolismo , Genética Populacional , Hipóxia/metabolismo , América do SulRESUMO
Apart from an outbreak in commercial poultry in Chile in 2002, there have been few reports of avian influenza in South America. However, surveillance in free-flying birds has been limited. An avian influenza virus was isolated from a Cinnamon Teal (Anas cyanoptera) in Bolivia in 2001 from samples collected for an avian influenza virus and avian paramyxovirus surveillance study. This isolate was determined to be an H7N3 virus by gene sequencing. Analysis of all eight genes revealed that five genes were most closely related to the H7N3 in Chile in 2002. Two genes were most closely related to North American wild aquatic bird virus lineages and one gene was most closely related to an equine influenza virus from South America.
Assuntos
Patos/virologia , Vírus da Influenza A Subtipo H3N8/genética , Vírus da Influenza A/genética , Vírus da Influenza A/isolamento & purificação , Influenza Aviária/virologia , Animais , Vírus da Influenza A/classificação , Influenza Aviária/epidemiologia , América do Norte , América do Sul/epidemiologiaRESUMO
An H7N3 avian influenza virus (AIV) was isolated from a Cinnamon Teal (Anas cyanoptera) (A/CinnamonTeal/Bolivia/4537/01) during a survey of wild waterfowl in Bolivia in 2001. The NA and M genes had the greatest identity with North American wild bird isolates, the NS was most closely related to an equine virus, and the remaining genes were most closely related to isolates from an outbreak of H7N3 in commercial poultry in Chile in 2002. The HA protein cleavage site and the results of pathogenesis studies in chickens were consistent with a low-pathogenicity virus, and the infective dose was 10(5) times higher for chickens than turkeys.