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1.
Mol Biol Evol ; 40(5)2023 05 02.
Artículo en Inglés | MEDLINE | ID: mdl-37146172

RESUMEN

Convergent adaptation to the same environment by multiple lineages frequently involves rapid evolutionary change at the same genes, implicating these genes as important for environmental adaptation. Such adaptive molecular changes may yield either change or loss of protein function; loss of function can eliminate newly deleterious proteins or reduce energy necessary for protein production. We previously found a striking case of recurrent pseudogenization of the Paraoxonase 1 (Pon1) gene among aquatic mammal lineages-Pon1 became a pseudogene with genetic lesions, such as stop codons and frameshifts, at least four times independently in aquatic and semiaquatic mammals. Here, we assess the landscape and pace of pseudogenization by studying Pon1 sequences, expression levels, and enzymatic activity across four aquatic and semiaquatic mammal lineages: pinnipeds, cetaceans, otters, and beavers. We observe in beavers and pinnipeds an unexpected reduction in expression of Pon3, a paralog with similar expression patterns but different substrate preferences. Ultimately, in all lineages with aquatic/semiaquatic members, we find that preceding any coding-level pseudogenization events in Pon1, there is a drastic decrease in expression, followed by relaxed selection, thus allowing accumulation of disrupting mutations. The recurrent loss of Pon1 function in aquatic/semiaquatic lineages is consistent with a benefit to Pon1 functional loss in aquatic environments. Accordingly, we examine diving and dietary traits across pinniped species as potential driving forces of Pon1 functional loss. We find that loss is best associated with diving activity and likely results from changes in selective pressures associated with hypoxia and hypoxia-induced inflammation.


Asunto(s)
Arildialquilfosfatasa , Caniformia , Animales , Arildialquilfosfatasa/genética , Mamíferos/genética , Cetáceos/genética , Roedores , Hipoxia
2.
Proc Natl Acad Sci U S A ; 116(26): 12913-12918, 2019 06 25.
Artículo en Inglés | MEDLINE | ID: mdl-31182611

RESUMEN

Hypoxia is a major physiological constraint for which multicellular eukaryotes have evolved robust cellular mechanisms capable of addressing dynamic changes in O2 availability. In animals, oxygen sensing and regulation is primarily performed by the hypoxia-inducible factor (HIF) pathway, and the key components of this pathway are thought to be highly conserved across metazoans. Marine intertidal habitats are dynamic environments, and their inhabitants are known to tolerate wide fluctuations in salinity, temperature, pH, and oxygen. In this study, we show that an abundant intertidal crustacean, the copepod Tigriopus californicus, has lost major genetic components of the HIF pathway, but still shows robust survivorship and transcriptional response to hypoxia. Mining of protein domains across the genome, followed by phylogenetic analyses of gene families, did not identify two key regulatory elements of the metazoan hypoxia response, namely the transcription factor HIF-α and its oxygen-sensing prolyl hydroxylase repressor, EGLN Despite this loss, phenotypic assays revealed that this species is tolerant to extremely low levels of available O2 for at least 24 h at both larval and adult stages. RNA-sequencing (seq) of copepods exposed to nearly anoxic conditions showed differential expression of over 400 genes, with evidence for induction of glycolytic metabolism without a depression of oxidative phosphorylation. Moreover, genes involved in chitin metabolism and cuticle reorganization show categorically a consistent pattern of change during anoxia, highlighting this pathway as a potential solution to low oxygen availability in this small animal with no respiratory structures or pigment.


Asunto(s)
Copépodos/genética , Factor 1 Inducible por Hipoxia/genética , Prolina Dioxigenasas del Factor Inducible por Hipoxia/genética , Oxígeno/metabolismo , Adaptación Fisiológica , Animales , Copépodos/metabolismo , Glucólisis , Factor 1 Inducible por Hipoxia/metabolismo , Prolina Dioxigenasas del Factor Inducible por Hipoxia/metabolismo , Transcriptoma
3.
Mol Biol Evol ; 37(5): 1342-1349, 2020 05 01.
Artículo en Inglés | MEDLINE | ID: mdl-32003807

RESUMEN

Metazoans respond to hypoxic stress via the hypoxia-inducible factor (HIF) pathway, a mechanism thought to be extremely conserved due to its importance in monitoring cellular oxygen levels and regulating responses to hypoxia. However, recent work revealed that key members of the HIF pathway have been lost in specific lineages (a tardigrade and a copepod), suggesting that this pathway is not as widespread in animals as previously assumed. Using genomic and transcriptomic data from 70 different species across 12 major crustacean groups, we assessed the degree to which the gene HIFα, the master regulator of the HIF pathway, was conserved. Mining of protein domains, followed by phylogenetic analyses of gene families, uncovered group-level losses of HIFα, including one across three orders within Cirripedia, and in three orders within Copepoda. For these groups, additional assessment showed losses of HIF repression machinery (EGLN and VHL). These results suggest the existence of alternative mechanisms for cellular response to low oxygen and highlight these taxa as models useful for probing these evolutionary outcomes.


Asunto(s)
Crustáceos/genética , Evolución Molecular , Subunidad alfa del Factor 1 Inducible por Hipoxia/genética , Prolina Dioxigenasas del Factor Inducible por Hipoxia/genética , Proteína Supresora de Tumores del Síndrome de Von Hippel-Lindau/genética , Animales
4.
Heredity (Edinb) ; 127(1): 107-123, 2021 07.
Artículo en Inglés | MEDLINE | ID: mdl-33903741

RESUMEN

Introgression of beneficial alleles has emerged as an important avenue for genetic adaptation in both plant and animal populations. In vertebrates, adaptation to hypoxic high-altitude environments involves the coordination of multiple molecular and cellular mechanisms, including selection on the hypoxia-inducible factor (HIF) pathway and the blood-O2 transport protein hemoglobin (Hb). In two Andean duck species, a striking DNA sequence similarity reflecting identity by descent is present across the ~20 kb ß-globin cluster including both embryonic (HBE) and adult (HBB) paralogs, though it was yet untested whether this is due to independent parallel evolution or adaptive introgression. In this study, we find that identical amino acid substitutions in the ß-globin cluster that increase Hb-O2 affinity have likely resulted from historical interbreeding between high-altitude populations of two different distantly-related species. We examined the direction of introgression and discovered that the species with a deeper mtDNA divergence that colonized high altitude earlier in history (Anas flavirostris) transferred adaptive genetic variation to the species with a shallower divergence (A. georgica) that likely colonized high altitude more recently possibly following a range shift into a novel environment. As a consequence, the species that received these ß-globin variants through hybridization might have adapted to hypoxic conditions in the high-altitude environment more quickly through acquiring beneficial alleles from the standing, hybrid-origin variation, leading to faster evolution.


Asunto(s)
Altitud , Globinas beta , Animales , Proteínas Portadoras , Evolución Molecular , Análisis de Secuencia de ADN , Globinas beta/genética , Globinas beta/metabolismo
5.
Mol Ecol ; 28(3): 584-599, 2019 02.
Artículo en Inglés | MEDLINE | ID: mdl-30548575

RESUMEN

The role of gene expression in adaptation to differing thermal environments has been assayed extensively. Yet, in most natural systems, analyses of gene expression reveal only one level of the complexity of regulatory machineries. MicroRNAs (miRNAs) are small noncoding RNAs which are key components of many gene regulatory networks, and they play important roles in a variety of cellular pathways by modulating post-transcriptional quantities of mRNA available for protein synthesis. The characterization of miRNA loci and their regulatory dynamics in nonmodel systems are still largely understudied. In this study, we examine the role of miRNAs in response to high thermal stress in the intertidal copepod Tigriopus californicus. Allopatric populations of this species show varying levels of local adaptation with respect to thermal regimes, and previous studies showed divergence in gene expression between populations from very different thermal environments. We examined the transcriptional response to temperature stress in two populations separated by only 8 km by utilizing RNA-seq to quantify both mRNA and miRNA levels. Using the currently available genome sequence, we first describe the repertoire of miRNAs in T. californicus and assess the degree to which transcriptional response to temperature stress is governed by miRNA activity. The two populations showed large differences in the number of genes involved, the magnitude of change in commonly used genes and in the number of miRNAs involved in transcriptional modulation during stress. Our results suggest that an increased level of regulatory network complexity may underlie improved survivorship under thermal stress in one of the populations.


Asunto(s)
Copépodos/genética , Genética de Población , Calor , MicroARNs/genética , Estrés Fisiológico , Adaptación Fisiológica/genética , Animales , California , Análisis de Secuencia de ARN , Transcriptoma
6.
Heredity (Edinb) ; 122(6): 819-832, 2019 06.
Artículo en Inglés | MEDLINE | ID: mdl-30631144

RESUMEN

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.


Asunto(s)
Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/genética , Patos/genética , Prolina Dioxigenasas del Factor Inducible por Hipoxia/genética , Aclimatación , Adaptación Fisiológica , Altitud , Animales , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/metabolismo , Patos/metabolismo , Exones , Humanos , Prolina Dioxigenasas del Factor Inducible por Hipoxia/metabolismo , Oxígeno/metabolismo , Selección Genética , América del Sur
7.
PLoS One ; 19(1): e0294842, 2024.
Artículo en Inglés | MEDLINE | ID: mdl-38170710

RESUMEN

Evidence from a variety of organisms points to convergent evolution on the mitochondria associated with a physiological response to oxygen deprivation or temperature stress, including mechanisms for high-altitude adaptation. Here, we examine whether demography and/or selection explains standing mitogenome nucleotide diversity in high-altitude adapted populations of three Andean waterfowl species: yellow-billed pintail (Anas georgica), speckled teal (Anas flavirostris), and cinnamon teal (Spatula cyanoptera). We compared a total of 60 mitogenomes from each of these three duck species (n = 20 per species) across low and high altitudes and tested whether part(s) or all of the mitogenome exhibited expected signatures of purifying selection within the high-altitude populations of these species. Historical effective population sizes (Ne) were inferred to be similar between high- and low-altitude populations of each species, suggesting that selection rather than genetic drift best explains the reduced genetic variation found in mitochondrial genes of high-altitude populations compared to low-altitude populations of the same species. Specifically, we provide evidence that establishment of these three Andean waterfowl species in the high-altitude environment, coincided at least in part with a persistent pattern of negative purifying selection acting on oxidative phosphorylation (OXPHOS) function of the mitochondria. Our results further reveal that the extent of gene-specific purifying selection has been greatest in the speckled teal, the species with the longest history of high-altitude occupancy.


Asunto(s)
Genoma Mitocondrial , Genoma Mitocondrial/genética , Altitud , Flujo Genético , Mitocondrias/genética , Ambiente , Adaptación Fisiológica/genética , Selección Genética
8.
Genome Biol Evol ; 15(1)2023 01 04.
Artículo en Inglés | MEDLINE | ID: mdl-36648250

RESUMEN

For aerobic organisms, both the hypoxia-inducible factor pathway and the mitochondrial genomes are key players in regulating oxygen homeostasis. Recent work has suggested that these mechanisms are not as highly conserved as previously thought, prompting more surveys across animal taxonomic levels, which would permit testing of hypotheses about the ecological conditions facilitating evolutionary loss of such genes. The Phylum Cnidaria is known to harbor wide variation in mitochondrial chromosome morphology, including an extreme example, in the Myxozoa, of mitochondrial genome loss. Because myxozoans are obligate endoparasites, frequently encountering hypoxic environments, we hypothesize that variation in environmental oxygen availability could be a key determinant in the evolution of metabolic gene networks associated with oxygen-sensing, hypoxia-response, and energy production. Here, we surveyed genomes and transcriptomes across 46 cnidarian species for the presence of HIF pathway members, as well as for an assortment of hypoxia, mitochondrial, and stress-response toolkit genes. We find that presence of the HIF pathway, as well as number of genes associated with mitochondria, hypoxia, and stress response, do not vary in parallel to mitochondrial genome morphology. More interestingly, we uncover evidence that myxozoans have lost the canonical HIF pathway repression machinery, potentially altering HIF pathway functionality to work under the specific conditions of their parasitic lifestyles. In addition, relative to other cnidarians, myxozoans show loss of large proportions of genes associated with the mitochondrion and involved in response to hypoxia and general stress. Our results provide additional evidence that the HIF regulatory machinery is evolutionarily labile and that variations in the canonical system have evolved in many animal groups.


Asunto(s)
Cnidarios , Myxozoa , Animales , Cnidarios/metabolismo , Oxígeno/metabolismo , Myxozoa/genética , Hipoxia/genética , Homeostasis , Subunidad alfa del Factor 1 Inducible por Hipoxia
9.
Genome Biol Evol ; 15(2)2023 02 03.
Artículo en Inglés | MEDLINE | ID: mdl-36718542

RESUMEN

Change in gene family size has been shown to facilitate adaptation to different selective pressures. This includes gene duplication to increase dosage or diversification of enzymatic substrates and gene deletion due to relaxed selection. We recently found that the PON1 gene, an enzyme with arylesterase and lactonase activity, was lost repeatedly in different aquatic mammalian lineages, suggesting that the PON gene family is responsive to environmental change. We further investigated if these fluctuations in gene family size were restricted to mammals and approximately when this gene family was expanded within mammals. Using 112 metazoan protein models, we explored the evolutionary history of the PON family to characterize the dynamic evolution of this gene family. We found that there have been multiple, independent expansion events in tardigrades, cephalochordates, and echinoderms. In addition, there have been partial gene loss events in monotremes and sea cucumbers and what appears to be complete loss in arthropods, urochordates, platyhelminths, ctenophores, and placozoans. In addition, we show the mammalian expansion to three PON paralogs occurred in the ancestor of all mammals after the divergence of sauropsida but before the divergence of monotremes from therians. We also provide evidence of a novel PON expansion within the brushtail possum. In the face of repeated expansions and deletions in the context of changing environments, we suggest a range of selective pressures, including pathogen infection and mitigation of oxidative damage, are likely influencing the diversification of this dynamic gene family across metazoa.


Asunto(s)
Artrópodos , Vertebrados , Animales , Vertebrados/genética , Proteínas/genética , Duplicación de Gen , Artrópodos/genética , Mamíferos , Evolución Molecular
10.
J Hered ; 103(3): 400-7, 2012.
Artículo en Inglés | MEDLINE | ID: mdl-22345645

RESUMEN

Environmental temperature plays a crucial role in determining a species distribution and abundance by affecting individual physiological processes, metabolic activities, and developmental rates. Many studies have identified clinal variation in phenotypes associated with response to environmental stresses, but variation in traits associated with climatic adaptation directly attributed to sequence variation within candidate gene regions has been difficult to identify. Insect heat shock genes are possible agents of thermal tolerance because of their involvement in protein folding, traffic, protection, and renaturation at the cellular level in response to temperature stress. Previously, members of the Drosophila small heat shock protein (sHSP) complex (Hsp23, Hsp26, Hsp27, Hsp67Ba) have been implicated as candidate climatic adaptation genes; therefore, this research examines sequence variation at these genes in 2 distant populations of Drosophila pseudoobscura. Flies from Tempe, AZ (n = 30) and Cheney, WA (n = 17) were used in the study. We identify high differentiation in the heat-shock complex (F(ST) : 0.219**, 0.262*, 0.279***, 0.166 not significant) as compared with neighboring genes and Tajima's D values indicative of balancing selection (Mann-Whitney U = 38, n(1) = 10 n(2) = 4, P < 0.05 two-tailed), both of which are suggestive of such climatic adaptation.


Asunto(s)
Proteínas de Drosophila/genética , Proteínas de Choque Térmico/genética , Adaptación Biológica/genética , Animales , Arizona , Clima , Drosophila , Evolución Molecular , Conversión Génica , Flujo Génico , Desequilibrio de Ligamiento , Masculino , Modelos Genéticos , Polimorfismo Genético , Selección Genética , Análisis de Secuencia de ADN , Washingtón
11.
BMC Evol Biol ; 11: 95, 2011 Apr 13.
Artículo en Inglés | MEDLINE | ID: mdl-21489230

RESUMEN

BACKGROUND: The reproductive ground plan hypothesis of social evolution suggests that reproductive controls of a solitary ancestor have been co-opted during social evolution, facilitating the division of labor among social insect workers. Despite substantial empirical support, the generality of this hypothesis is not universally accepted. Thus, we investigated the prediction of particular genes with pleiotropic effects on ovarian traits and social behavior in worker honey bees as a stringent test of the reproductive ground plan hypothesis. We complemented these tests with a comprehensive genome scan for additional quantitative trait loci (QTL) to gain a better understanding of the genetic architecture of the ovary size of honey bee workers, a morphological trait that is significant for understanding social insect caste evolution and general insect biology. RESULTS: Back-crossing hybrid European x Africanized honey bee queens to the Africanized parent colony generated two study populations with extraordinarily large worker ovaries. Despite the transgressive ovary phenotypes, several previously mapped QTL for social foraging behavior demonstrated ovary size effects, confirming the prediction of pleiotropic genetic effects on reproductive traits and social behavior. One major QTL for ovary size was detected in each backcross, along with several smaller effects and two QTL for ovary asymmetry. One of the main ovary size QTL coincided with a major QTL for ovary activation, explaining 3/4 of the phenotypic variance, although no simple positive correlation between ovary size and activation was observed. CONCLUSIONS: Our results provide strong support for the reproductive ground plan hypothesis of evolution in study populations that are independent of the genetic stocks that originally led to the formulation of this hypothesis. As predicted, worker ovary size is genetically linked to multiple correlated traits of the complex division of labor in worker honey bees, known as the pollen hoarding syndrome. The genetic architecture of worker ovary size presumably consists of a combination of trait-specific loci and general regulators that affect the whole behavioral syndrome and may even play a role in caste determination. Several promising candidate genes in the QTL intervals await further study to clarify their potential role in social insect evolution and the regulation of insect fertility in general.


Asunto(s)
Abejas/genética , Evolución Biológica , Sitios de Carácter Cuantitativo , Animales , Abejas/anatomía & histología , Abejas/fisiología , Conducta Animal , Femenino , Tamaño de los Órganos , Ovario/anatomía & histología , Ovario/fisiología , Reproducción
12.
Genome Biol Evol ; 10(1): 14-32, 2018 01 01.
Artículo en Inglés | MEDLINE | ID: mdl-29211852

RESUMEN

Local adaptation frequently occurs across populations as a result of migration-selection balance between divergent selective pressures and gene flow associated with life in heterogeneous landscapes. Studying the effects of selection and gene flow on the adaptation process can be achieved in systems that have recently colonized extreme environments. This study utilizes an endemic South American duck species, the speckled teal (Anas flavirostris), which has both high- and low-altitude populations. High-altitude speckled teal (A. f. oxyptera) are locally adapted to the Andean environment and mostly allopatric from low-altitude birds (A. f. flavirostris); however, there is occasional gene flow across altitudinal gradients. In this study, we used next-generation sequencing to explore genetic patterns associated with high-altitude adaptation in speckled teal populations, as well as the extent to which the balance between selection and migration have affected genetic architecture. We identified a set of loci with allele frequencies strongly correlated with altitude, including those involved in the insulin-like signaling pathway, bone morphogenesis, oxidative phosphorylation, responders to hypoxia-induced DNA damage, and feedback loops to the hypoxia-inducible factor pathway. These same outlier loci were found to have depressed gene flow estimates, as well as being highly concentrated on the Z-chromosome. Our results suggest a multifactorial response to life at high altitudes through an array of interconnected pathways that are likely under positive selection and whose genetic components seem to be providing an effective genomic barrier to interbreeding, potentially functioning as an avenue for population divergence and speciation.


Asunto(s)
Aclimatación , Patos/genética , Patos/fisiología , Flujo Génico , Flujo Genético , Adaptación Fisiológica , Altitud , Migración Animal , Animales , Polimorfismo de Nucleótido Simple , Selección Genética
13.
PLoS One ; 12(6): e0179545, 2017.
Artículo en Inglés | MEDLINE | ID: mdl-28614393

RESUMEN

Hypoxia inducible factor (HIF) transcription factors are crucial for regulating a variety of cellular activities in response to oxygen stress (hypoxia). In this study, we determine the evolutionary history of HIF genes and their associated transactivation domains, as well as perform selection and functional divergence analyses across their four characteristic domains. Here we show that the HIF genes are restricted to metazoans: At least one HIF-α homolog is found within the genomes of non-bilaterians and bilaterian invertebrates, while most vertebrate genomes contain between two and six HIF-α genes. We also find widespread purifying selection across all four characteristic domain types, bHLH, PAS, NTAD, CTAD, in HIF-α genes, and evidence for Type I functional divergence between HIF-1α, HIF-2α /EPAS, and invertebrate HIF genes. Overall, we describe the evolutionary histories of the HIF transcription factor gene family and its associated transactivation domains in eukaryotes. We show that the NTAD and CTAD domains appear de novo, without any appearance outside of the HIF-α subunits. Although they both appear in invertebrates as well as vertebrate HIF- α sequences, there seems to have been a substantial loss across invertebrates or were convergently acquired in these few lineages. We reaffirm that HIF-1α is phylogenetically conserved among most metazoans, whereas HIF-2α appeared later. Overall, our findings can be attributed to the substantial integration of this transcription factor family into the critical tasks associated with maintenance of oxygen homeostasis and vascularization, particularly in the vertebrate lineage.


Asunto(s)
Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/genética , Eucariontes/genética , Variación Genética , Selección Genética , Vertebrados/genética , Animales , Factores de Transcripción con Motivo Hélice-Asa-Hélice Básico/clasificación , Eucariontes/clasificación , Evolución Molecular , Humanos , Subunidad alfa del Factor 1 Inducible por Hipoxia/clasificación , Subunidad alfa del Factor 1 Inducible por Hipoxia/genética , Filogenia , Vertebrados/clasificación
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