Evolution of pinniped UCP1 is not linked to aquatic life but to neonatal thermogenesis and body size.
Ontology highlight
ABSTRACT:
SUBMITTER: Gaudry MJ
PROVIDER: S-EPMC8833166 | biostudies-literature | 2022 Feb
REPOSITORIES: biostudies-literature
Publications
Evolution of pinniped UCP1 is not linked to aquatic life but to neonatal thermogenesis and body size.
Gaudry Michael J MJ Fyda Thomas Jacob TJ Jastroch Martin M
Proceedings of the National Academy of Sciences of the United States of America 20220201 6
Similar Datasets
Project description:BackgroundUncoupling protein 1 (UCP1) is a mitochondrial anion carrier, expressed in brown adipose tissue (BAT) of Eutherians. UCP1 is responsible for uncoupling mitochondrial proton transport from the production of ATP, thereby dissipating heat; it is essential for non-shivering thermogenesis (NST) in mammalian BAT. UCP1 orthologs have been identified in non-Eutherian mammals, fish and amphibians. Yet, UCP1 has a unique function in Eutherians in that it is necessary in the production of heat (NST). As such, this study aims to determine the evolutionary mode of UCP1 in Eutherians, where there is clear evidence of UCP1-dependent NST in BAT.ResultsModels of adaptive evolution through phylogenetic analysis of amino acid sequences by maximum likelihood were implemented to determine the mode of UCP1 protein evolution in Eutherians. An increase in the rate of amino acid substitutions on the branch leading to Eutherians is observed, but is best explained by relaxed constraints, not positive selection. Further, evidence for branch and site heterogeneity in selection pressures, as well as divergent selection pressures between UCP1 and its paralogs (UCP2-3) is observed.ConclusionWe propose that the unique thermogenic function of UCP1 in Eutherians may be best explained by neutral processes. Along with other evidence, this suggests that the primary biochemical properties of UCP1 may not differ between Eutherians and non-Eutherians.
| S-EPMC2627829 | biostudies-literature
Project description:Intraspecific phenotypic variation is a significant component of biodiversity. Body size, for example, is variable and critical for structuring communities. We need to understand how homogenous and variably sized populations differ in their ecological responses or effects if we are to have a robust understanding of communities. We manipulated body size variation in consumer (tadpole) populations in mesocosms (both with and without predators), keeping mean size and density of these consumers constant. Size-variable consumer populations exhibited stronger antipredator responses (reduced activity), which had a cascading effect of increasing the biomass of the consumer's resources. Predators foraged less when consumers were variable in size, and this may have mediated the differential effects of predators on the community composition of alternative prey (zooplankton). All trophic levels responded to differences in consumer size variation, demonstrating that intrapopulation phenotypic variability can significantly alter interspecific ecological interactions. Furthermore, we identify a key mechanism (size thresholds for predation risk) that may mediate impacts of size variation in natural communities. Together, our results suggest that phenotypic variability plays a significant role in structuring ecological communities.
| S-EPMC5723604 | biostudies-literature
Project description:It has recently been proposed that life-history evolution is subject to a fundamental size-dependent constraint. This constraint limits the rate at which biomass can be produced so that production per unit of body mass is inevitably slower in larger organisms than in smaller ones. Here we derive predictions for how changes in body size and production rates evolve in different lifestyles subject to this constraint. Predictions are tested by using data on the mass of neonate tissue produced per adult per year in 637 placental mammal species and are generally supported. Compared with terrestrial insectivores with generalized primitive traits, mammals that have evolved more specialized lifestyles have divergent mass-specific production rates: (i) increased in groups that specialize on abundant and reliable foods: grazing and browsing herbivores (artiodactyls, lagomorphs, perissodactyls, and folivorous rodents) and flesh-eating marine mammals (pinnipeds, cetaceans); and (ii) decreased in groups that have lifestyles with reduced death rates: bats, primates, arboreal, fossorial, and desert rodents, bears, elephants, and rhinos. Convergent evolution of groups with similar lifestyles is common, so patterns of productivity across mammalian taxa reflect both ecology and phylogeny. The overall result is that groups with different lifestyles have parallel but offset relationships between production rate and body size. These results shed light on the evolution of the fast-slow life-history continuum, suggesting that variation occurs along two axes corresponding to body size and lifestyle.
| S-EPMC2077039 | biostudies-literature
Project description:Brown adipocytes are unique in that they expend energy and produce heat to maintain euthermia through expression of uncoupling protein-1 (UCP1). Given their propensity to stimulate weight loss and promote resistance to obesity, they are a compelling interventional target for obesity-related disorders. Here, we tested whether an optogenetic approach could be used to activate UCP1-dependent thermogenesis in brown adipocytes. We generated brown adipocytes expressing a bacterial-derived photoactivatable adenylyl cyclase (bPAC) that, upon blue light stimulation, increases UCP1 expression, fuel uptake and thermogenesis. This unique system allows for precise, chemical free, temporal control of UCP1-dependent thermogenesis, which can aid in our understanding of brown adipocyte biology and development of therapies that target obesity-related disorders.
| S-EPMC10139976 | biostudies-literature
Project description:Thermogenesis by uncoupling protein 1 (UCP1) is one of the primary mechanisms by which brown adipose tissue (BAT) increases energy expenditure. UCP1 resides in the inner mitochondrial membrane (IMM), where it dissipates membrane potential independent of adenosine triphosphate (ATP) synthase. Here, we provide evidence that phosphatidylethanolamine (PE) modulates UCP1-dependent proton conductance across the IMM to modulate thermogenesis. Mitochondrial lipidomic analyses revealed PE as a signature molecule whose abundance bidirectionally responds to changes in thermogenic burden. Reduction in mitochondrial PE by deletion of phosphatidylserine decarboxylase (PSD) made mice cold intolerant and insensitive to β3 adrenergic receptor agonist-induced increase in whole-body oxygen consumption. High-resolution respirometry and fluorometry of BAT mitochondria showed that loss of mitochondrial PE specifically lowers UCP1-dependent respiration without compromising electron transfer efficiency or ATP synthesis. These findings were confirmed by a reduction in UCP1 proton current in PE-deficient mitoplasts. Thus, PE performs a previously unknown role as a temperature-responsive rheostat that regulates UCP1-dependent thermogenesis.
| S-EPMC9956115 | biostudies-literature
Project description:The study of life history variation is central to the evolutionary theory. In many ectothermic lineages, including lizards, life history traits are plastic and relate to several sources of variation including body size, which is both a factor and a life history trait likely to modulate reproductive parameters. Larger species within a lineage, for example tend to be more fecund and have larger clutch size, but clutch size may also be influenced by climate, independently of body size. Thus, the study of climatic effects on lizard fecundity is mandatory on the current scenario of global climatic change. We asked how body and clutch size have responded to climate through time in a group of tropical lizards, the Tropidurinae, and how these two variables relate to each other. We used both traditional and phylogenetic comparative methods. Body and clutch size are variable within Tropidurinae, and both traits are influenced by phylogenetic position. Across the lineage, species which evolved larger size produce more eggs and neither trait is influenced by temperature components. A climatic component of precipitation, however, relates to larger female body size, and therefore seems to exert an indirect relationship on clutch size. This effect of precipitation on body size is likely a correlate of primary production. A decrease in fecundity is expected for Tropidurinae species on continental landmasses, which are predicted to undergo a decrease in summer rainfall.
| S-EPMC3094402 | biostudies-literature
Project description:Mammals have two types of thermogenic adipocytes: brown adipocytes and beige adipocytes. Thermogenic adipocytes express high levels of uncoupling protein 1 (UCP1) to dissipates energy in the form of heat by uncoupling the mitochondrial proton gradient from mitochondrial respiration. There is much evidence that UCP1 is the center of BAT thermogenesis and systemic energy homeostasis. Recently, UCP1 independent thermogenic pathway identified in thermogenic adipocytes. Importantly, the thermogenic pathways are different in brown and beige adipocytes. Ca2+-ATPase 2b calcium cycling mechanism is selective to beige adipocytes. It remains unknown how the multiple thermogenic mechanisms are coordinately regulated. The discovery of UCP1-independent thermogenic mechanisms potential offer new opportunities for improving obesity and type 2 diabetes particularly in groups such as elderly and obese populations who do not possess UCP1 positive adipocytes.
| S-EPMC7399049 | biostudies-literature
Project description:The activation of thermogenesis in adipose tissue has emerged as an important target for the development of novel anti-obesity therapies. Using multi-well isothermal microcalorimetry, we have demonstrated that mature murine brown and brite adipocytes produce quantifiable heat upon β3-AR stimulation, independently of any anaerobic mechanisms. Additionally, in brite adipocytes lacking UCP1 protein, β3-AR stimulation still induces heat production, albeit to a much lower extent than in their wildtype counterparts, suggesting that UCP1 is an essential component of adrenergic induced thermogenesis in murine brite adipocytes exvivo. Similarly, we could observe an increase in heat production in human-derived adipocytes (hMADS) upon β-AR stimulation. Collectively, these results establish the use of isothermal microcalorimetry as a sensitive and accurate technique for measuring thermogenic responses in intact mature brite adipocytes from murine and human origin.
| S-EPMC8455563 | biostudies-literature
Project description:BackgroundOrganism biomass is one of the most important variables in ecological studies, making biomass estimations one of the most common laboratory tasks. Biomass of small macroinvertebrates is usually estimated as dry mass or ash-free dry mass (hereafter 'DM' vs. 'AFDM') per sample; a laborious and time consuming process, that often can be speeded up using easily measured and reliable proxy variables like body size or wet (fresh) mass. Another common way of estimating AFDM (one of the most accurate but also time-consuming estimates of biologically active tissue mass) is the use of AFDM/DM ratios as conversion factors. So far, however, these ratios typically ignore the possibility that the relative mass of biologically active vs. non-active support tissue (e.g., protective exoskeleton or shell)-and therefore, also AFDM/DM ratios-may change with body size, as previously shown for taxa like spiders, vertebrates and trees.MethodsWe collected aquatic, epibenthic macroinvertebrates (>1 mm) in 32 shallow bays along a 360 km stretch of the Swedish coast along the Baltic Sea; one of the largest brackish water bodies on Earth. We then estimated statistical relationships between the body size (length or height in mm), body dry mass and ash-free dry mass for 14 of the most common taxa; five gastropods, three bivalves, three crustaceans and three insect larvae. Finally, we statistically estimated the potential influence of body size on the AFDM/DM ratio per taxon.ResultsFor most taxa, non-linear regression models describing the power relationship between body size and (i) DM and (ii) AFDM fit the data well (as indicated by low SE and high R2). Moreover, for more than half of the taxa studied (including the vast majority of the shelled molluscs), body size had a negative influence on organism AFDM/DM ratios.DiscussionThe good fit of the modelled power relationships suggests that the constants reported here can be used to quickly estimate organism dry- and ash-free dry mass based on body size, thereby freeing up considerable work resources. However, the considerable differences in constants between taxa emphasize the need for taxon-specific relationships, and the potential dangers associated with ignoring body size. The negative influence of body size on the AFDM/DM ratio found in a majority of the molluscs could be caused by increasingly thicker shells with organism age, and/or spawning-induced loss of biologically active tissue in adults. Consequently, future studies utilizing AFDM/DM (and presumably also AFDM/wet mass) ratios should carefully assess the potential influence of body size to ensure more reliable estimates of organism body mass.
| S-EPMC5270594 | biostudies-literature
Project description:Secondarily aquatic tetrapods have many unique morphologic adaptations for life underwater compared with their terrestrial counterparts. A key innovation during the land-to-water transition was feeding. Pinnipeds, a clade of air-breathing marine carnivorans that include seals, sea lions, and walruses, have evolved multiple strategies for aquatic feeding (e.g., biting, suction feeding). Numerous studies have examined the pinniped skull and dental specializations for underwater feeding. However, data on the pinniped craniofacial musculoskeletal system and its role in aquatic feeding are rare. Therefore, the objectives of this study were to conduct a comparative analysis of pinniped craniofacial musculature and examine the function of the craniofacial musculature in facilitating different aquatic feeding strategies. We performed anatomic dissections of 35 specimens across six pinniped species. We describe 32 pinniped craniofacial muscles-including facial expression, mastication, tongue, hyoid, and soft palate muscles. Pinnipeds broadly conform to mammalian patterns of craniofacial muscle morphology. Pinnipeds also exhibit unique musculoskeletal morphologies-in muscle position, attachments, and size-that likely represent adaptations for different aquatic feeding strategies. Suction feeding specialists (bearded and northern elephant seals) have a significantly larger masseter than biters. Further, northern elephant seals have large and unique tongue and hyoid muscle morphologies compared with other pinniped species. These morphologic changes likely help generate and withstand suction pressures necessary for drawing water and prey into the mouth. In contrast, biting taxa (California sea lions, harbor, ringed, and Weddell seals) do not exhibit consistent craniofacial musculoskeletal adaptations that differentiate them from suction feeders. Generally, we discover that all pinnipeds have well-developed and robust craniofacial musculature. Pinniped head musculature plays an important role in facilitating different aquatic feeding strategies. Together with behavioral and kinematic studies, our data suggest that pinnipeds' robust facial morphology allows animals to switch feeding strategies depending on the environmental context-a critical skill in a heterogeneous and rapidly changing underwater habitat.
| S-EPMC8742965 | biostudies-literature