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1.
Mol Biol Evol ; 39(11)2022 11 03.
Artigo em Inglês | MEDLINE | ID: mdl-36288802

RESUMO

Mitochondrial (mt) and nuclear-encoded proteins are integrated in aerobic respiration, requiring co-functionality among gene products from fundamentally different genomes. Different evolutionary rates, inheritance mechanisms, and selection pressures set the stage for incompatibilities between interacting products of the two genomes. The mitonuclear coevolution hypothesis posits that incompatibilities may be avoided if evolution in one genome selects for complementary changes in interacting genes encoded by the other genome. Nuclear compensation, in which deleterious mtDNA changes are offset by compensatory nuclear changes, is often invoked as the primary mechanism for mitonuclear coevolution. Yet, direct evidence supporting nuclear compensation is rare. Here, we used data from 58 mammalian species representing eight orders to show strong correlations between evolutionary rates of mt and nuclear-encoded mt-targeted (N-mt) proteins, but not between mt and non-mt-targeted nuclear proteins, providing strong support for mitonuclear coevolution across mammals. N-mt genes with direct mt interactions also showed the strongest correlations. Although most N-mt genes had elevated dN/dS ratios compared to mt genes (as predicted under nuclear compensation), N-mt sites in close contact with mt proteins were not overrepresented for signs of positive selection compared to noncontact N-mt sites (contrary to predictions of nuclear compensation). Furthermore, temporal patterns of N-mt and mt amino acid substitutions did not support predictions of nuclear compensation, even in positively selected, functionally important residues with direct mitonuclear contacts. Overall, our results strongly support mitonuclear coevolution across ∼170 million years of mammalian evolution but fail to support nuclear compensation as the major mode of mitonuclear coevolution.


Assuntos
DNA Mitocondrial , Genes Mitocondriais , Animais , DNA Mitocondrial/genética , Mamíferos/genética , Núcleo Celular/genética , Proteínas Mitocondriais/genética , Genômica
2.
Am Nat ; 202(4): E121-E129, 2023 10.
Artigo em Inglês | MEDLINE | ID: mdl-37792916

RESUMO

AbstractDisentangling different types of selection is a common goal in molecular evolution. Elevated dN/dS ratios (the ratio of nonsynonymous to synonymous substitution rates) in focal lineages are often interpreted as signs of positive selection. Paradoxically, relaxed purifying selection can also result in elevated dN/dS ratios, but tests to distinguish these two causes are seldomly implemented. Here, we reevaluated seven case studies describing elevated dN/dS ratios in animal mitochondrial DNA (mtDNA) and their accompanying hypotheses regarding selection. They included flightless lineages versus flighted lineages in birds, bats, and insects and physiological adaptations in snakes, two groups of electric fishes, and primates. We found that elevated dN/dS ratios were often not caused by the predicted mechanism, and we sometimes found strong support for the opposite mechanism. We discuss reasons why energetic hypotheses may be confounded by other selective forces acting on mtDNA and caution against overinterpreting singular molecular signals, including elevated dN/dS ratios.


Assuntos
Genoma Mitocondrial , Animais , Filogenia , Seleção Genética , Evolução Molecular , Primatas/genética , DNA Mitocondrial/genética
3.
Biol Lett ; 16(9): 20200450, 2020 09.
Artigo em Inglês | MEDLINE | ID: mdl-32933406

RESUMO

Mitochondrial (mt) respiration depends on proteins encoded both by the mitochondrial and nuclear genomes. Variation in mt-DNA mutation rates exists across eukaryotes, although the functional consequences of elevated mt mutation rates in some lineages remain underexplored. In the angiosperm genus Silene, closely related, ecologically similar species have either 'fast' or 'slow' mt-DNA mutation rates. Here, we investigated the functional consequences of elevated mt-DNA mutation rates on mt respiration profiles of Silene mitochondria. Overall levels of respiration were similar among Species. Fast species had lower respiration efficiency than slow species and relied up to 48% more on nuclear-encoded respiratory enzymes alternative oxidase (AOX) and accessory dehydrogenases (DHex), which participate in stress responses in plants. However, not all fast species showed these trends. Respiratory profiles of some enzymes were correlated, most notably AOX and DHex. We conclude that subtle differences in mt physiology among Silene lineages with dramatically different mt mutation rates may underly similar phenotypes at higher levels of biological organization, betraying the consequences of mt mutations.


Assuntos
Silene , DNA Mitocondrial , Evolução Molecular , Genoma de Planta , Mitocôndrias/genética , Proteínas Mitocondriais/genética , Mutação , Taxa de Mutação , Silene/genética
4.
J Exp Biol ; 222(Pt 12)2019 06 25.
Artigo em Inglês | MEDLINE | ID: mdl-31160425

RESUMO

An animal's pace of life is mediated by the physiological demands and stressors it experiences (e.g. reproduction) and one likely mechanism that underlies these effects is oxidative stress. Reproduction has been shown to increase or reduce oxidative stress under different conditions and to modify mitochondrial performance. We hypothesized that the changes associated with reproduction can alter how animals respond to future oxidative stressors. We tested this theory by comparing the organ-specific mitochondrial response in wild-derived female house mice. Specifically, we examined the effect of an oxidant (X-irradiation) on virgin mice and on mice that had reproduced. We measured liver and skeletal muscle mitochondrial density, respiratory performance, enzyme activity and oxidant production, as well as markers of oxidative damage to tissues. In the liver, prior reproduction prevented a radiation-induced reduction in mitochondrial density and increased mitochondrial respiratory performance. In skeletal muscle, prior reproduction resulted in a radiation-induced decline in mitochondrial density which could reduce the bioenergetic capacity of skeletal muscle mitochondria. Yet, electron transport chain complex I activity in skeletal muscle, which dropped after reproduction, returned to control levels following oxidant exposure. The results of this investigation indicate that prior reproduction alters the response of mitochondria to an oxidative challenge in an organ-specific manner. Such changes could have differential effects on future reproductive performance and risk of death.


Assuntos
Fígado/efeitos da radiação , Mitocôndrias/fisiologia , Músculo Esquelético/efeitos da radiação , Estresse Oxidativo , Reprodução , Raios X/efeitos adversos , Animais , Feminino , Fígado/fisiologia , Camundongos , Mitocôndrias/efeitos da radiação , Músculo Esquelético/fisiologia , Oxirredução , Paridade
5.
J Exp Biol ; 221(Pt 15)2018 08 13.
Artigo em Inglês | MEDLINE | ID: mdl-29941616

RESUMO

Carotenoids are well known for their contribution to the vibrant coloration of many animals and have been hypothesized to be important antioxidants. Surprisingly few examples of carotenoids acting as biologically relevant antioxidants in vivo exist, in part because experimental designs often employ carotenoid doses at levels that are rarely observed in nature. Here, we used an approach that reduces carotenoid content from wild-type levels to test for the effect of carotenoids as protectants against an oxidative challenge. We used the marine copepod Tigriopus californicus reared on a carotenoid-free or a carotenoid-restored diet of nutritional yeast and then exposed them to a pro-oxidant. We found that carotenoid-deficient copepods not only accumulated more damage but also were more likely to die during an oxidative challenge than carotenoid-restored copepods. We suggest that carotenoid reduction, and not supplementation, better tests the proposed roles of carotenoids in other physiological functions in animals.


Assuntos
Antioxidantes/farmacologia , Copépodes/efeitos dos fármacos , Estresse Oxidativo/efeitos dos fármacos , Zeaxantinas/farmacologia , Animais , Dieta , terc-Butil Hidroperóxido/farmacologia
6.
Biochim Biophys Acta Bioenerg ; 1864(4): 149003, 2023 11 01.
Artigo em Inglês | MEDLINE | ID: mdl-37557975

RESUMO

The alternative oxidase (AOX) is a terminal oxidase in the electron transport system that plays a role in mitochondrial bioenergetics. The past 20 years of research shows AOX has a wide yet patchy distribution across the tree of life. AOX has been suggested to have a role in stress tolerance, growth, and development in plants, but less is known about its function in other groups, including animals. In this study, we analyzed the taxonomic distribution of AOX across >2800 species representatives from prokaryotes and eukaryotes and developed a standardized workflow for finding and verifying the authenticity of AOX sequences. We found that AOX is limited to proteobacteria among prokaryotes, but is widely distributed in eukaryotes, with the highest prevalence in plants, fungi, and protists. AOX is present in many invertebrates, but is absent in others including most arthropods, and is absent from vertebrates. We found aberrant AOX sequences associated with some animal groups. Some of these aberrant AOXs were contaminants, but we also found putative cases of lateral gene transfer of AOX from fungi and protists to nematodes, springtails, fungus gnats, and rotifers. Our findings provide a robust and detailed analysis of the distribution of AOX and a method for identifying and verifying putative AOX sequences, which will be useful as more sequence data becomes available on public repositories.


Assuntos
Transferência Genética Horizontal , Proteínas de Plantas , Animais , Proteínas de Plantas/genética , Oxirredutases/genética , Mitocôndrias/genética , Plantas , Eucariotos/genética
7.
Biol Rev Camb Philos Soc ; 98(6): 2320-2332, 2023 12.
Artigo em Inglês | MEDLINE | ID: mdl-37563787

RESUMO

Even as numerous studies have documented that the red and yellow coloration resulting from the deposition of carotenoids serves as an honest signal of condition, the evolution of condition dependency is contentious. The resource trade-off hypothesis proposes that condition-dependent honest signalling relies on a trade-off of resources between ornamental display and body maintenance. By this model, condition dependency can evolve through selection for a re-allocation of resources to promote ornament expression. By contrast, the index hypothesis proposes that selection focuses mate choice on carotenoid coloration that is inherently condition dependent because production of such coloration is inexorably tied to vital cellular processes. These hypotheses for the origins of condition dependency make strongly contrasting and testable predictions about ornamental traits. To assess these two models, we review the mechanisms of production of carotenoids, patterns of condition dependency involving different classes of carotenoids, and patterns of behavioural responses to carotenoid coloration. We review evidence that traits can be condition dependent without the influence of sexual selection and that novel traits can show condition-dependent expression as soon as they appear in a population, without the possibility of sexual selection. We conclude by highlighting new opportunities for studying condition-dependent signalling made possible by genetic manipulation and expression of ornamental traits in synthetic biological systems.


Assuntos
Carotenoides , Pigmentação , Carotenoides/metabolismo , Pigmentação/fisiologia
8.
J R Soc Interface ; 19(190): 20220169, 2022 05.
Artigo em Inglês | MEDLINE | ID: mdl-35611618

RESUMO

While the specific mechanisms of colour production in biological systems are diverse, the mechanics of colour production are straightforward and universal. Colour is produced through the selective absorption of light by pigments, the scattering of light by nanostructures or a combination of both. When Tigriopus californicus copepods were fed a carotenoid-limited diet of yeast, their orange-red body coloration became faint, but their eyespots remained unexpectedly bright red. Raman spectroscopy indicated a clear signature of the red carotenoid pigment astaxanthin in eyespots; however, refractive index matching experiments showed that eyespot colour disappeared when placed in ethyl cinnamate, suggesting a structural origin for the red coloration. We used transmission electron microscopy to identify consecutive nanolayers of spherical air pockets that, when modelled as a single thin film layer, possess the correct periodicity to coherently scatter red light. We then performed microspectrophotometry to quantify eyespot coloration and confirmed a distinct colour difference between the eyespot and the body. The observed spectral reflectance from the eyespot matched the reflectance predicted from our models when considering the additional absorption by astaxanthin. Together, this evidence suggests the persistence of red eyespots in copepods is the result of a combination of structural and pigmentary coloration.


Assuntos
Copépodes , Animais , Carotenoides , Microscopia Eletrônica de Transmissão , Organelas , Pigmentação
9.
PLoS One ; 16(11): e0259371, 2021.
Artigo em Inglês | MEDLINE | ID: mdl-34748608

RESUMO

The marine copepod, Tigriopus californicus, produces the red carotenoid pigment astaxanthin from yellow dietary precursors. This 'bioconversion' of yellow carotenoids to red is hypothesized to be linked to individual condition, possibly through shared metabolic pathways with mitochondrial oxidative phosphorylation. Experimental inter-population crosses of lab-reared T. californicus typically produces low-fitness hybrids is due in large part to the disruption of coadapted sets nuclear and mitochondrial genes within the parental populations. These hybrid incompatibilities can increase variability in life history traits and energy production among hybrid lines. Here, we tested if production of astaxanthin was compromised in hybrid copepods and if it was linked to mitochondrial metabolism and offspring development. We observed no clear mitonuclear dysfunction in hybrids fed a limited, carotenoid-deficient diet of nutritional yeast. However, when yellow carotenoids were restored to their diet, hybrid lines produced less astaxanthin than parental lines. We observed that lines fed a yeast diet produced less ATP and had slower offspring development compared to lines fed a more complete diet of algae, suggesting the yeast-only diet may have obscured effects of mitonuclear dysfunction. Astaxanthin production was not significantly associated with development among lines fed a yeast diet but was negatively related to development in early generation hybrids fed an algal diet. In lines fed yeast, astaxanthin was negatively related to ATP synthesis, but in lines fed algae, the relationship was reversed. Although the effects of the yeast diet may have obscured evidence of hybrid dysfunction, these results suggest that astaxanthin bioconversion may still be related to mitochondrial performance and reproductive success.


Assuntos
Carotenoides/metabolismo , Copépodes/genética , Aptidão Genética , Animais , Organismos Aquáticos , Núcleo Celular/genética , Núcleo Celular/metabolismo , Copépodes/metabolismo , Hibridização Genética , Invertebrados , Mitocôndrias/genética , Mitocôndrias/metabolismo , Fosforilação Oxidativa , Xantofilas/metabolismo
10.
Biol Bull ; 238(2): 119-130, 2020 04.
Artigo em Inglês | MEDLINE | ID: mdl-32412843

RESUMO

Red coloration is a widely distributed phenotype among animals, yet the pigmentary and genetic bases for this phenotype have been described in relatively few taxa. Here we show that the Hawaiian endemic anchialine shrimp Halocaridina rubra is red because of the accumulation of astaxanthin. Laboratory colonies of phylogenetically distinct lineages of H. rubra have colony-specific amounts of astaxanthin that are developmentally, and likely genetically, fixed. Carotenoid supplementation and restriction experiments failed to change astaxanthin content from the within-colony baseline levels, suggesting that dietary limitation is not a major factor driving coloration differences. A possible candidate gene product predicted to be responsible for the production of astaxanthin in H. rubra and other crustaceans is closely related to the bifunctional cytochrome P450 family 3 enzyme CrtS found in fungi. However, homologs to the enzyme thought to catalyze ketolation reactions in birds and turtles, CYP2J19, were not found. This work is one of the first steps in linking phenotypic variation in red coloration of H. rubra to genotypic variation. Future work should focus on (1) pinpointing the genes that function in the bioconversion of dietary carotenoids to astaxanthin, (2) examining what genomic variants might drive variation in coloration among discrete lineages, and (3) testing more explicitly for condition-dependent carotenoid coloration in crustaceans.


Assuntos
Carotenoides , Pigmentação , Animais , Aves , Variação Genética , Havaí
11.
Integr Comp Biol ; 59(4): 994-1004, 2019 10 01.
Artigo em Inglês | MEDLINE | ID: mdl-30912813

RESUMO

The environment in which eukaryotes first evolved was drastically different from what they experience today, and one of the key limiting factors was the availability of oxygen for mitochondrial respiration. During the transition to a fully oxygenated Earth, other compounds such as sulfide posed a considerable constraint on using mitochondrial aerobic respiration for energy production. The ancestors of animals, and those that first evolved from the simpler eukaryotes have mitochondrial respiratory components that are absent from later-evolving animals. Specifically, mitochondria of most basal metazoans have a sulfide-resistant alternative oxidase (AOX), which provides a secondary oxidative pathway to the classical cytochrome pathway. In this essay, I argue that because of its resistance to sulfide, AOX respiration was critical to the evolution of animals by enabling oxidative metabolism under otherwise inhibitory conditions. I hypothesize that AOX allowed for metabolic flexibility during the stochastic oxygen environment of early Earth which shaped the evolution of basal metazoans. I briefly describe the known functions of AOX, with a particular focus on the decreased production of reactive oxygen species (ROS) during stress conditions. Then, I propose three evolutionary consequences of AOX-mediated protection from ROS observed in basal metazoans: 1) adaptation to stressful environments, 2) the persistence of facultative sexual reproduction, and 3) decreased mitochondrial DNA mutation rates. Recognizing the diversity of mitochondrial respiratory systems present in animals may help resolve the mechanisms involved in major evolutionary processes such as adaptation and speciation.


Assuntos
Adaptação Biológica/fisiologia , Mitocôndrias/enzimologia , Oxirredutases/genética , Animais , Oxirredução , Oxirredutases/metabolismo , Espécies Reativas de Oxigênio/metabolismo , Estresse Fisiológico
12.
Integr Comp Biol ; 59(4): 856-863, 2019 10 01.
Artigo em Inglês | MEDLINE | ID: mdl-31504533

RESUMO

Eukaryotes are the outcome of an ancient symbiosis and as such, eukaryotic cells fundamentally possess two genomes. As a consequence, gene products encoded by both nuclear and mitochondrial genomes must interact in an intimate and precise fashion to enable aerobic respiration in eukaryotes. This genomic architecture of eukaryotes is proposed to necessitate perpetual coevolution between the nuclear and mitochondrial genomes to maintain coadaptation, but the presence of two genomes also creates the opportunity for intracellular conflict. In the collection of papers that constitute this symposium volume, scientists working in diverse organismal systems spanning vast biological scales address emerging topics in integrative, comparative biology in light of mitonuclear interactions.


Assuntos
Coevolução Biológica , Núcleo Celular/fisiologia , Eucariotos/fisiologia , Genoma Mitocondrial/fisiologia , Adaptação Biológica , Núcleo Celular/genética , Eucariotos/genética , Genoma Mitocondrial/genética
13.
Nat Commun ; 9(1): 73, 2018 01 08.
Artigo em Inglês | MEDLINE | ID: mdl-29311592

RESUMO

Thirty years of research has made carotenoid coloration a textbook example of an honest signal of individual quality, but tests of this idea are surprisingly inconsistent. Here, to investigate sources of this heterogeneity, we perform meta-analyses of published studies on the relationship between carotenoid-based feather coloration and measures of individual quality. To create color displays, animals use either carotenoids unchanged from dietary components or carotenoids that they biochemically convert before deposition. We hypothesize that converted carotenoids better reflect individual quality because of the physiological links between cellular function and carotenoid metabolism. We show that feather coloration is an honest signal of some, but not all, measures of quality. Where these relationships exist, we show that converted, but not dietary, carotenoid coloration drives the relationship. Our results have broad implications for understanding the evolutionary role of carotenoid coloration and the physiological mechanisms that maintain signal honesty of animal ornamental traits.


Assuntos
Carotenoides/metabolismo , Cor , Plumas/metabolismo , Pigmentação , Aves Canoras/metabolismo , Animais , Doenças das Aves/parasitologia , Dieta , Resistência à Doença , Plumas/química , Feminino , Interações Hospedeiro-Parasita , Masculino , Reprodução , Aves Canoras/classificação , Aves Canoras/parasitologia , Especificidade da Espécie
14.
Philos Trans R Soc Lond B Biol Sci ; 372(1724)2017 Jul 05.
Artigo em Inglês | MEDLINE | ID: mdl-28533460

RESUMO

Many of the colour displays of animals are proposed to have evolved in response to female mate choice for honest signals of quality, but such honest signalling requires mechanisms to prevent cheating. The most widely accepted and cited mechanisms for ensuring signal honesty are based on the costly signalling hypothesis, which posits that costs associated with ornamentation prevent low-quality males from being highly ornamented. Alternatively, by the index hypothesis, honesty can be achieved via cost-free mechanisms if ornament production is causally linked to core physiological pathways. In this essay, we review how a costly signalling framework has shaped empirical research in mate choice for colourful male ornaments and emphasize that alternative interpretations are plausible under an index signalling framework. We discuss the challenges in both empirically testing and distinguishing between the two hypotheses, noting that they need not be mutually exclusive. Finally, we advocate for a comprehensive approach to studies of colour signals that includes the explicit consideration of cost-free mechanisms for honesty.This article is part of the themed issue 'Animal coloration: production, perception, function and application'.


Assuntos
Comunicação Animal , Evolução Biológica , Cor , Preferência de Acasalamento Animal , Animais , Feminino , Masculino , Pigmentação
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