how are birds and mammals alike

School of Life Sciences, Northeast Normal University, 5268 Renmin Street, Changchun 130024, Peoples Republic of China

Jilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, Northeast Normal University, 2555 Jingyue Street, Changchun 130117, Peoples Republic of China

School of Life Sciences, Northeast Normal University, 5268 Renmin Street, Changchun 130024, Peoples Republic of China

Jilin Provincial Key Laboratory of Animal Resource Conservation and Utilization, Northeast Normal University, 2555 Jingyue Street, Changchun 130117, Peoples Republic of China

The diapsid lineage (birds) and synapsid lineage (mammals), share a suite of functionally similar characteristics (e.g. endothermy) that are considered to be a result of their convergent evolution, but the candidate selections leading to this convergent evolution are still under debate. Here, we used a newly developed molecular phyloecological approach to reconstruct the diel activity pattern of the common ancestors of living birds. Our results strongly suggest that they had adaptations to nocturnality during their early evolution, which is remarkably similar to that of ancestral mammals. Given their similar adaptation to nocturnality, we propose that the shared traits in birds and mammals may have partly evolved as a result of the convergent evolution of their early ancestors adapting to ecological factors (e.g. low ambient temperature) associated with nocturnality. Finally, a conceptually unifying ecological model on the evolution of endothermy in diverse organisms with an emphasis on low ambient temperature is proposed. We reason that endothermy may evolve as an adaptive strategy to enable organisms to effectively implement various life-cycle activities under relatively low-temperature environments. In particular, a habitat shift from high-temperature to relatively low-temperature environments is identified as a common factor underlying the evolution of endothermy.

Extant birds and mammals share a number of highly similar characteristics, including but not limited to, enhanced hearing, vocal communication, endothermy, insulation, shivering, respiratory turbinates, high basal metabolism, grinding, sustained activity, four-chambered heart, high blood pressure, and intensive parental care [1–8]. These bird-mammal shared characteristics (BMSC) are considered to have evolved convergently in the two groups [4], while the selection pressures that underlie their convergent evolution are still under debate. To date, many candidate selections, which are not necessarily mutually exclusive, have been proposed [9–11] and popular views suggest that BMSC (e.g. endothermy) evolved primarily for increased sustained activity [1] and enhanced parental care [4,5]. On the other hand, the traditional view, the thermal niche expansion model, proposes that nocturnality may have facilitated the evolution of endothermy in ancestral mammals that would not necessarily feature a high resting metabolic rate typical of most living mammals [2,8]. Indeed, early mammals are widely accepted as having been nocturnal [12,13], and it has been hypothesized that the evolution of endothermy may have allowed them to overcome ambient low-temperature constraints to be active at night, while diurnal ectothermic reptiles essentially depend on sunlight to increase their body temperature to operational levels [12,14]. The nocturnality hypothesis is criticized as being suitable only to mammals [1], partly because so far only the nocturnality of the synapsid lineages (e.g. early mammals) is well known, while the possible nocturnal activity of the diapsid lineages (e.g. birds), especially during their early evolution, is unknown.

The diel activity pattern of ancestral birds has received less attention. To date, there are only two relevant studies based on behaviour or morphology analyses. A maximum-likelihood reconstruction based on behavioural data suggests the diurnality of the common ancestor of living birds (CALB) [15]. This study classifies each species as either diurnal or nocturnal without consideration of other behavioural possibilities (e.g. crepuscular or cathemeral) or behavioural complexity, for instance, the widespread existence of the occasional nocturnality of typically diurnal birds [16], and hence this result may be less accurate. Another study uses a phylogenetic discriminant analysis to reconstruct the diel activity patterns of four fossil basal birds (Archaeopteryx lithographica, Confuciusornis sanctus, Sapeornis chaoyangensis, Yixianornis grabaui) based on eye morphology data, and the result demonstrates their diurnality [17]. The phylogenetic discriminant analysis approach is criticized for its inability to distinguish diurnality from cathemerality (i.e. active both day and night) [18,19], and hence uncertainty remains concerning the diel activity patterns of these basal birds. Given the uncertainties of the results, the diel activity pattern of ancestral birds remains unclear.

The recent development of a molecular phyloecological (MPE) approach allows us to reconstruct the diel activity pattern of ancestral taxa using molecular data [13,20–22]. The MPE approach has been applied to analyse the diel activity patterns of birds and mammals, and the results demonstrate its sensitivity to distinct animals with different diel activity patterns, showing that nocturnality, diurnality, and cathemerality are featured by enhanced positive selection of dim-light vision genes (rod-expressed genes), bright-light vision genes (cone-expressed genes), and both, respectively [13,20,22]. In this study, we employed the MPE approach to reconstruct the early evolution of the diel activity patterns in diapsid lineages. Our results reveal that diapsid lineages exhibit similar nocturnality adaption to that of synapsid lineages. Our findings provide insights into the candidate selection that underlies the convergent evolution of the shared characteristics, especially endothermy, in birds and mammals.

Both red and white blood cells, known as leukocytes and erythrocytes, are found in the blood of mammals and birds, respectively. Both classes of animals’ red blood cells are made of hemoglobin, an iron-containing protein that carries oxygen and gives blood its red hue. Although erythrocytes are found in both classes, erythrocytes from mammals do not have nuclei, whereas erythrocytes from birds do. The leukocytes of both classes function in immune regulation.

The fact that both classes of mammals and birds provide for their young after they hatch or are born is another similarity between them. Depending on when the young of a species are first able to care for themselves, the amount of time varies. Mammals that are lactating use their mammary glands to produce milk, which is used to nourish their young. Birds will catch and occasionally predigest food for their young in the interim.

Birds, mammals, and all other animal species have continued to expand in novel and fascinating ways throughout the course of evolutionary history. There are birds that can hover in the air, such as hummingbirds, birds that are flightless, such as ostriches in Africa, emus in Australia, and kiwis in New Zealand, and birds that are seafaring, such as penguins that can only swim.

Birds have evolved to metabolize energy and oxygen slightly differently than mammals, but they both use the process of cellular respiration to do so. Lungs are used by mammals’ respiratory systems to breathe in and out while absorbing oxygen from the atmosphere. In contrast, birds’ lungs and unique air sac membranes enable them to absorb and release oxygen from their bodies more quickly.

Because they have warm blood, both birds and mammals are able to regulate their body temperature and do not require the presence of an outside heat source to stay warm. This similarity gives rise to a number of other similarities, including comparable caloric needs based on weight and the capacity to stay active in colder climates. Although they don’t need to eat as much, cold-blooded animals like reptiles cannot withstand lower temperatures. Additionally, mammals and birds have the rare capacity to survive on any landmass on Earth because they are warm-blooded. Because of these adaptations, birds and other animals belong to some of the most diverse and abundant classes in the animal kingdom.

2. Results and discussion

Following the MPE approach for studying the diel activity pattern of ancestral taxa [13,20–22], we reconstructed the diel activity patterns of our focal taxa by analysing the adaptive evolution of 33 phototransduction genes (electronic supplementary material, table S1) involved in the rod and cone phototransduction pathway [23,24] in the context of sauropsid phylogeny (figure 1). Positively selected genes were identified based on the branch-site model (electronic supplementary material, table S2), and the positive selection remained robust when phylogenetic uncertainties [25,37,38] (electronic supplementary material, tables S3 and S4) and initial value variations of kappa and ? were considered.

Figure 1. Diel activity pattern reconstruction. The phylogenetic relationships of species used in this study follows published literature [25–36] and the Tree of Life Web Project (http://tolweb.org/Passeriformes). The diel activity classification of taxonomic bird orders follows one published study [16]. Red shows bird orders involved in nocturnal and/or crepuscular activities. Except for five regularly nocturnal bird groups, which harbour mainly nocturnally active species, all other bird groups are considered as typically diurnal, but widely show occasional nocturnality or engage in partial behaviours during crepuscular periods [16].

First, we looked at the phototransduction genes’ adaptive evolution along the branch that connects all living birds to a common ancestor. GRK1, a gene expressed by rods, exhibited the strongest positive selection signal (? = 13). 983, d. f. = 1, p = 0. 002) (electronic supplementary material, table S2 and figure S1), as well as SLC24A1, a different rod-expressed gene, demonstrated a marginally significant positive selection signal (? = 25). 293, d. f. = 1, p = 0. 053). Rods’ activated rhodopsin is inactivated by rhodopsin kinase, or GRK1. Cyclic guanosine monophosphate (cGMP) concentration can be restored by extruding free calcium in the outer segment of rods, which is facilitated by SLC24A1, which encodes the Na/Ca2-K exchanger. Both genes help detect motion and are involved in photoresponse recovery [39]. The discovery of positive selection signals in the two rod-expressed genes points to the CALB’s notably improved capacity for motion detection in low light (e g. nocturnality). Additionally, we discovered that PDE6C, a cone-expressed gene, was positively selected (? = 26). 734, d. f. = 1, p = 0. 014). The hydrolytic subunits of cGMP phosphodiesterase (PDE6) are encoded by PDE6C in cones, and it is well known that PDE6C is essential for signal amplification in the phototransduction cascade. Cone-expressed genes are positively selected, indicating increased selection for improved visual acuity in bright light conditions (e g. diurnality). Our results indicating positive selections for both the cone- and rod-expressed genes imply that the CALB may have been active during the day and that they may have developed a better ability to detect motion at night.

In crepuscular conditions, where both rods and cones are functionally active, the combined positive selection of the genes expressing both rods and cones may also be selected for mesopic vision. We then looked at the potential spectral tuning of four cone opsin genes, LWS, RH2, SWS2, and SWS1, in the CALB to see if there are shifts in their wavelengths of maximal absorption (?max) towards the relatively abundant short-wavelength light in twilight, which characterizes crepuscularly active animals [13,20]. No critical amino acid replacement was discovered along the CALB branch among the critical amino acid sites (electronic supplementary material, table S5) that have been studied and are linked to the spectral tuning of cone opsins [40–43], indicating that the likelihood of the spectral tuning of the cone opsins changing is low. This could imply that the CALB was mostly active during the day and at night (e g. cathemeral) rather than being mainly active crepuscularly. This is in line with a prior morphological study that demonstrated the orbital characteristics of the early stem bird species, Archaeopteryx lithographica, to be somewhat intermediate between nocturnality and diurnality [44].

Additionally, we recreated the diel activity pattern of an extinct archosaur, one of the farther-off CALBs. Interestingly, we discovered that two genes, GUCY2D and RCVRN, which are both rod- and cone-expressed and involved in phototransduction activation or photoresponse recovery, as well as four rod-expressed genes, CNGA1, GNAT1, PDE6B, and SLC24A1, were under positive selection along the ancestral archosaur branch (electronic supplementary material, table S2). In line with earlier research, the positive selection of the primarily rod-expressed genes implies improved visual acuity and motion detection in low light, which strongly suggests that the ancestral archosaur was most likely nocturnal [13,15,17]. Additionally, these positively selected genes include nearly all of the essential elements of the phototransduction pathway (electronic supplementary material, figure S2), indicating that the ancestral archosaur’s visual system underwent a significant alteration as a result of its adaptation to nocturnality. This discovery bears striking similarities to that of ancestral mammals [13].

Altogether, our molecular reconstruction based on the phylogenetic analysis by maximum likelihood (PAML) results suggests that while the CALB may have been active both night and day, the ancestral archosaur was more likely nocturnal (figure 1). When the branch site-unrestricted statistical test for episodic diversification (BUSTED) was used to confirm the selection signals of these positively selected genes identified by PAML, one rod-expressed gene (SLC24A1) and one cone-expressed gene (PDE6C) along the ancestral bird branch and three rod-expressed genes (CNGA1, PDE6B, and SLC24A1) along the ancestral archosaur branch were found to be under positive selection (electronic supplementary material, table S6), providing further support for our reconstructed diel activity results of our focal taxa. In light of these robust reconstructions, our molecular results and previous studies [13,17] consistently suggest that the diapsid lineages may have experienced strong adaptation to nocturnality, in parallel with the synapsid lineages (e.g. early mammals) [13]. The similar evolution of nocturnality in both diapsid and synapsid lineages should be considered as a derived result through their independent and convergent evolution, given that one previous study shows that the ancestral amniote and ancestral reptile were predominately diurnal (figure 2) [13].

Figure 2. Reconstructed diel activity patterns of main groups of amniotes based on the results of this study and previous studies [13,45]. Living endothermic groups and their possible early evolution of endothermy are shown in red based on previous studies [7,46–51].

Our molecular findings imply that the CALB may have gone through some nocturnal periods. Furthermore bolstering this nocturnality are numerous morphological and behavioral lines of evidence. (i) Based on eye morphology, theropod dinosaurs—one of the CALB—are reconstructed as primarily scotopic/cathemeral, indicating that the dinosaur ancestors of birds were primarily active in low light [17]. Numerous theropod dinosaurs have been found to have endothermy or mesothermy as well as feathers (insulation), which would allow them to be active at low temperatures during the night and are therefore consistent with their nocturnality [46, 52, 53]. (ii) Despite significant disagreement over taxonomy, Protoavis texensis—once thought to be the earliest bird—has owl-like, large, forward-facing orbits that suggest it is a nocturnal species [54]. (iii) Despite the fact that the majority of avian species are thought to be primarily nocturnal, they frequently demonstrate the capacity for nocturnal activity (e g. night migration) (figure 1) [16,55], in line with the CALB’s potential nocturnal behavior (iv) Of all terrestrial vertebrates, birds have the largest eyes [56]. Big eyes are typically associated with better visual acuity and are a feature of nocturnal taxa [16,57,58]. (v) Compared to reptiles, birds have developed vocal communication and far more sensitive hearing [3], indicating a greater reliance on acoustic communication, which is typically found in nocturnal species [57,58]. The nocturnality of the CALB is strongly supported by our molecular results as well as behavioural and morphological evidence, which contradicts its pure diurnality perspectives [15, 17]. While the precise reasons behind the nocturnality of CALBs are unknown, the nocturnality of ancestral mammals is typically attributed to competition with and/or predation by diurnal reptiles, such as g. dinosaurs) [59–61].

Crompton et al. suggested that the nocturnality of synapsid lineages, like mammals, may have aided in the evolution of endothermy [2]. In a similar vein, we suggest that nocturnality may have helped the evolution of endothermy in diapsid lineages as well, given that similar nocturnal adaptations have been discovered in ancestral birds, theropod dinosaurs, and archosaurs [17] (figure 1). Previous research supports this by showing that the evolution of endothermy in diapsids can be traced back to basal archosaurs [46–48] or even earlier to non-avian dinosaurs [7,46,62,63]. Specifically, the fact that both crocodiles and birds have a four-chambered heart raises the possibility that basal archosaurs also evolved a four-chambered heart, supporting the possibility of their endothermy [48]. Likewise, it has been established that synapsid lineages became nocturnal considerably earlier (e g. their endothermy has been shown to have evolved much earlier than true mammals as well, and may be traced back to the common ancestor of Neotherapsida, more than 260 Ma [7,49–51]. the Late Carboniferous, nearly 300 Ma) than true mammals [45]. Considering this, it seems that the development of endothermy in the diapsid and synapsid lineages corresponds with the emergence of their nocturnality, endorsing the nocturnality theory as a plausible explanation for their endothermy evolution. Birds and mammals share many other traits in addition to endothermy, and it is still unclear when the two lineages’ independent evolution began. Upcoming palaeobiological discoveries could shed light on when they originated and help comprehend how nocturnality might have affected their evolution.

The diapsid (e.g. birds) and synapsid (e.g. mammals) lineages share many functionally similar characteristics, such as enhanced hearing, vocal communication, endothermy, insulation, shivering, respiratory turbinates, high basal metabolism, grinding, sustained activity, four-chambered heart, high blood pressure, and intensive parental care [1–8]. The possible integrated and correlated evolution of these BMSC has long been recognized [1,4,8,14]. Here, we attempt to explain their possible integrated evolution in the context of the adaptation to nocturnality (figure 3).

Figure 3. Integrated evolution of bird-mammal shared characteristics for adapting to nocturnality. Arrows show possible cause and effect relationships between two nocturnality-associated selection pressures (visual constraints and low temperature) and the evolution of BMSC. Please see text for details. The black background represents dim-light environments (e.g. night) and red represents the evolution of endothermy-related characteristics under low-temperature selection pressure. BMR, basal metabolic rate.

Two fundamental constraints: the limitation of visual function and the low ambient temperature, may have exerted significant selection pressure for integrated evolution of the BMSC during the transition from a diurnal to nocturnal amniote (reptile) ancestor (figure 2). Due to compensatory selection pressure in low light, non-visual senses like improved hearing and vocal communication may evolve as a result of the visual functional constraints. Nocturnal animals typically possess highly developed non-visual senses, which lends support to this [57,58,64]. Previous research indicates that the low temperature selection pressure could result in the evolution of respiratory turbinates, insulation (fur and feathers), endothermy, or even shivering. Given that many life-cycle activities are temperature-dependent [14], endothermy has long been thought of as an adaptive strategy to cold temperatures [2,8,65–68]. It is thought that insulation (fur and feathers) and respiratory turbinates prevent heat loss [4,7,8]. Shivering may then develop to produce more heat for a quick rise in core temperature. Endothermy is thought to be partially associated with high basal metabolic rate (BMR) [1], even though its underlying thermogenesis mechanism is not fully understood. This may then call for both adequate food supply and accelerated assimilation, such as grinding by mastication in mammals and in the gizzard in birds [8]. The increased need for food may therefore influence the selection of more sustained, high-intensity activities for effective food acquisition. An adequate oxygen supply is necessary for both high BMR and sustained activity, which may have resulted in the evolution of the four chambered heart, high blood pressure, and other related anatomical structures [4].

The two choices—the restriction on visual function and the low outside temperature linked to nocturnality—may have also aided in the development of intensive parental care. Due to its higher surface area to volume ratio, a juvenile with a small body size has obvious disadvantages on cold nights. Intensive parental care is therefore necessary to lower the mortality rate of offspring [8]. Endothermy, hearing, and vocal communication would all be further enhanced by the benefits of parental care, increasing the likelihood that the offspring would survive the night [4]. In spite of this, it is thought that providing for children during their early years comes at a high cost, which could put further selection pressure on continued activity to get more food [4,5]. Apart from facilitating foraging, prolonged physical exertion invariably produces heat (activity thermogenesis) [1,69] and could serve as a significant thermogenesis source that promotes endothermy. Activity thermogenesis may have functioned as one of the three primary thermogenesis sources contributing to endothermy, along with thermogenesis from BMR and shivering, ensuring the execution of diverse life-cycle activities in low-temperature environments. When considered collectively, the evolution of BMSC is consistent with nocturnality (figure 3), and it’s possible that BMSC evolved as a result of birds and mammals convergently adapting to particular nocturnality-associated selections.

Our findings imply that the nocturnal low-temperature selection pressure may have aided in the evolution of endothermy in the diapsid and synapsid lineages. Interestingly, low temperature is also thought to have influenced the evolution of regional endothermy in fishes, despite some disagreement on this point. g. lamnid sharks, billfishes, and tunas). Since these fish have adapted to live in warm water, it has been suggested that their endothermy may have originated from a number of oceanic cooling events that have occurred since the Eocene [65–67]. Similarly, it is discovered that the endothermic leatherback turtle (Dermochelys coriacea) has low-temperature dependent endogenous thermogenesis [70]. Given that facultative endothermy was found in at least two reptiles during the reproductive stage—the Indian python and the tegu lizard—low temperature may have also contributed to the evolution of this trait [71, 72]. Given that the Indian python only begins to produce heat for incubation when the outside temperature falls below a critical low temperature of 33°C [71], there may be a connection between the occurrence of relatively low outside temperatures and the development of facultative endothermy. Furthermore, certain explanations for the appearance of endothermy in endothermic insects and plants have taken into account the impact of low surrounding temperatures [73–75]. If the temperature of their surroundings consistently matched their high body temperature, it is possible that none of these endotherms would have evolved to produce heat on their own.

Parental care and sustained activity, which are commonly regarded as the initial selection pressures for the evolution of endothermy [1,4,5], may only be partial consequences of selection for various life-cycle activities under low-temperature conditions, rather than the sole or even the initial selective target, given the possibility that endothermy will evolve due to low temperatures (figure 3). There is criticism of the two popular views elsewhere [4,5,76]. Another problem is that no explanation is given as to why only the avian and mammalian lineages were chosen for continuous activity or intense parental care, while other living reptiles have not exhibited the same behavior. It is also suggested that body-size miniaturization, which happens concurrently throughout the evolutionary histories of both mammalian and avian lineages, plays a role in the emergence of endothermy, in addition to parental care and prolonged activity [68,77]. However, the miniaturization model is criticized elsewhere [9]. Rather than explaining the causes, the model was actually first applied to interpret how endothermy may evolve in mammals, and the underlying reason may have something to do with the nocturnality of ancestral mammals [68]. Furthermore, earlier research shows that endothermy evolved before miniaturization occurred in both the avian and mammalian lineages [68,77,78], indicating that miniaturization of body size may not have been the primary selection factor for endothermy’s evolution. It would be biased to highlight just one of the many possible biological functions of endothermy in relation to these various models of its evolution, which would result in numerous theoretical models that are only applicable to particular groups [9,11]. For example, the evolution of regional endothermy in fishes, which are known to have evolved for purposes other than sustained activity or parental care [65,67], is not explained by the models of aerobic capacity [1] or parental care [4]. The truth is that endothermy serves a wide range of purposes for all endothermic organisms that have been discovered to date. These purposes include locomotion, sensory communication, foraging, digestion, reproduction, breeding, antipredation, and parental care [1,4,14,65,67,73]. To explain the emergence of endothermy in a variety of organisms, a conceptually coherent model that takes into account all of these various functions of endothermy in the context of low-temperature environments would make more sense. Given this, we suggest that endothermy could develop as an adaptive strategy to allow organisms to carry out a variety of life-cycle tasks (e.g., g. parental care and sustained activity) under relatively low-temperature environments.

Figure 2 shows that the diapsid and synapsid lineages’ diel activity changes suggest that they may have undergone a habitat shift from high-temperature (day) to relatively low-temperature (night) environments. This shift may have aided in the evolution of their endothermy. In a similar vein, it has been proposed that the transition of diverse fishes from warm-water to cold-water habitat may have aided in the evolution of endothermy in those species [65–67]. Similarly, for leatherback turtles, the transition from tropical nesting sites to chilly northern foraging grounds is linked to the emergence of their endothermy [70]. One molecular phylogeographic study suggests that the facultative endothermic reptile, the Indian python (Python molurus) [71], may have originated in West Africa before spreading to Europe and Asia [79]. This suggests that the Indian python’s evolutionary origin may have involved a shift in habitat from high-temperature areas (tropical climate) to relatively low-temperature areas (subtropical/temperate climate) In comparison to its closest relatives, the salvator duseni and salvator rufescens, [80], the tegu lizard (Salvator merianae) [72], which extends its geographic distribution from tropical, subtropical to relatively low-temperature, temperate climates, may have undergone a similar high-to-low temperature habitat shift.

Based on these results, a common factor that appears to underpin the evolution of endothermy in these endothermic vertebrates appears to be a shift in habitat from high-temperature to relatively low-temperature environments. This particular shift in habitat could be a key factor in encouraging vertebrates to evolve endothermy. For enzymes and other molecules that had adapted to earlier, comparatively high-temperature conditions, endothermy would be preferentially favored in low-temperature environments. If this is the case, endothermy should be more common in taxa whose biogeographical histories involve a habitat shift from regions with high temperatures to those with relatively low temperatures. In relevant endothermic vertebrates, insects, and plants, this pattern still needs to be tested [73, 75].

It’s possible that endothermy isn’t the only adaptation for low temperatures. Alternative physiological or behavioral responses to cold temperatures may exist because certain ectothermic animals, such as geckos and cold-water fish, appear to be able to remain active in these conditions. Low temperature is just one of many potential variables that could influence the evolution of endothermy, including body size, food availability, biogeographic history, and the strength of selection. Future research should clarify why endothermy is limited to a few distinct groups by comparing and analyzing potential factors between endotherms and their phylogenetically closest ectotherms.

Strong evidence for the diapsid lineages’ nocturnality is presented in this study, which is consistent with the synapsid lineages’ behavior. An integrated viewpoint on the evolution of BMSC as a convergent adaptation to nocturnality is put forth in light of their nocturnality. Furthermore, low temperature is proposed as a potential common factor underlying endothermy evolution in vertebrates after summarizing our findings and pertinent empirical studies on the evolution of endothermy. A conceptually cohesive ecological model of endothermy evolution with a focus on low temperature is suggested in light of the importance of low temperature in endothermy evolution. As a habitat shifts from a high-temperature environment to a relatively low-temperature environment, we reason that endothermy may have evolved as an adaptive strategy to allow organisms to carry out various life-cycle activities under relatively low-temperature environments.

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