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Cytochrome b evolution in birds and mammals: an evaluation of the avian constraint hypothesis.

Patterns of molecular evolution in birds have long been considered anomalous. Compared with other vertebrates, birds have reduced levels of genetic divergence between groups of similar taxonomic ranks for a variety of nuclear and mitochondrial markers. This observation led to the avian constraint hypothesis, which identifies increased functional constraint on avian proteins as the cause for the reduction in genetic divergence. Subsequent investigations provided additional support for the avian constraint hypothesis when rates of molecular evolution were found to be slower in birds than in mammals in a variety of independent calibrations. It is possible to test the avian constraint hypothesis as an explanation for this avian slowdown by comparing DNA sequence data from protein-coding regions in birds and homologous regions in mammals. The increased selective constraints should lead to a reduction in the proportion of amino acid replacement substitutions. To test for such a decrease, we calculated the numbers of amino acid replacement substitutions per replacement site (dN) and silent substitutions per silent site (dS) for the complete mitochondrial cytochrome b gene using 38 avian and 43 mammalian comparisons that were phylogenetically independent. We find that dN/dS is significantly smaller in birds than in mammals. This difference cannot be explained by differences in codon bias affecting dS values. We suggest that the avian slowdown can be explained, at least in part, by a decreased tolerance for amino acid substitutions in avian species relative to mammalian species.

Animals↗

Protein evolution in different cellular environments: cytochrome b in sharks and mammals.

DNA sequences for the mitochondrial cytochrome b gene were determined for 13 species of sharks. Rates and patterns of amino acid replacement are compared for sharks and mammals. Absolute rates of cytochrome b evolution are six times slower in sharks than in mammals. Bivariate plots of the number of nonsynonymous and silent transversions are indistinguishable in the two groups, however, suggesting that the differences in amino acid replacement rates are due primarily to differences in DNA substitution rates. Patterns of amino acid replacement are also similar in the two groups. Conserved and variable regions occur in the same parts of the cytochrome b gene, and there is little evidence that the types of amino acid changes are significantly different between the groups. Similarity in the relative rates and patterns of protein change between the two groups prevails despite dramatic differences in the cellular environments of sharks and mammals. Poor penetrance of physiological differences through to rates of protein evolution provides support for the neutral theory and suggests that, for cytochrome b, patterns of evolution have been relatively constant throughout much of vertebrate history.

Amino Acid Sequence↗

Origin of the tooth-replacement pattern in therian mammals: evidence from a 110 Myr old fossil.

Living placental and marsupial mammals (therians) use distinctive tooth-replacement patterns that have not yet been traced back fully to their time of divergence in the Early Cretaceous (>100 Myr ago). Slaughteria eruptens, a small 110 Myr old fossil mammal from Texas, USA, is near the base of that divergence. Using ultra-high-resolution X-ray CT analysis we demonstrate that Slaughteria preserves an unrecognized pattern of tooth replacement with simple posterior premolars replacing molariform precursors. Differing from both placentals that have a more complex posterior adult premolar, and from marsupials, in which only one premolar is replaced, Slaughteria provides the first direct evidence of a tooth-replacement pattern that is plausible for the common ancestor of all therians. By our interpretation Slaughteria has only one adult molar in place and contains two mental foramina in the jaw, thus changing characters that are critical to reconstruction of mammalian relationships and to species discrimination and interpretations of diversity for Early Cretaceous mammals.

Animals↗

Determinants of loss of mammal species during the Late Quaternary 'megafauna' extinctions: life history and ecology, but not body size.

Extinctions of megafauna species during the Late Quaternary dramatically reduced the global diversity of mammals. There is intense debate over the causes of these extinctions, especially regarding the extent to which humans were involved. Most previous analyses of this question have focused on chronologies of extinction and on the archaeological evidence for human-megafauna interaction. Here, I take an alternative approach: comparison of the biological traits of extinct species with those of survivors. I use this to demonstrate two general features of the selectivity of Late Quaternary mammal extinctions in Australia, Eurasia, the Americas and Madagascar. First, large size was not directly related to risk of extinction; rather, species with slow reproductive rates were at high risk regardless of their body size. This finding rejects the 'blitzkrieg' model of overkill, in which extinctions were completed during brief intervals of selective hunting of large-bodied prey. Second, species that survived despite having low reproductive rates typically occurred in closed habitats and many were arboreal or nocturnal. Such traits would have reduced their exposure to direct interaction with people. Therefore, although this analysis rejects blitzkrieg as a general scenario for the mammal megafauna extinctions, it is consistent with extinctions being due to interaction with human populations.

Animals↗

Female multiple mating behaviour, early reproductive failure and litter size variation in mammals.

Female promiscuity is widespread among mammals, although its function is poorly understood. Recently, much interest has been generated by the hypothesis that female promiscuity, combined with post-copulatory paternity-biasing mechanisms, may function to reduce the costs of reproductive failure resulting from genetic incompatibility. Here, a comparative approach is used to determine if average rates of reproductive failure differ for polytocous mammal species with contrasting levels of female multiple-mating behaviour. After control for phylogeny, promiscuous species were found to have significantly lower rates of early reproductive failure than monogamous and polygynous species, in which females are relatively monandrous. Monandrous females appear to compensate for higher early reproductive failure with increased ova production, and thus produce comparable average litter sizes to those of more promiscuous females. However, there is significantly more variation around the average litter sizes produced by relatively monandrous females. These findings are broadly consistent with predictions of the genetic incompatibility avoidance hypothesis, although it is emphasized that alternative explanations cannot be ruled out on the basis of the comparative evidence presented. Further studies are needed to explore ecological correlates of multiple-mating behaviour, to investigate potential post-copulatory paternity-biasing mechanisms, and to identify the causes of reproductive failure in natural mammal populations.

Animals↗

Scaling laws for capillary vessels of mammals at rest and in exercise.

A general derivation is presented for the scaling laws governing the size and number of capillary blood vessels in mammals. The derivation is based on the assumption of three idealized similarity principles known to apply, at least approximately, to resting mammals: (i) size-invariant blood pressure; (ii) size-invariant fraction of blood in the capillaries; and (iii) size-invariant oxygen consumption and uptake, per unit of body mass, during each heart cycle. Results indicate that the radius and length of capillaries, and the number that are open and active in the resting state, should scale with mammal mass to the powers 1/12, 5/24 and 5/8, respectively, consistent with earlier work by the author. Measurements are presented supporting the results. Physiological changes accompanying strenuous exercise are accounted for by a change in the scaling law for capillary number, from scaling exponent 5/8 to 3/4.

Animals↗

Evolution of mammals: lactation helps mothers to cope with unreliable food supplies.

Lactation is a ubiquitous feature of mammalian reproduction. Because lactating females can draw on their nutrient reserves for milk production, it offers mothers and their dependent young independence from fluctuations in their food supplies. However, converting food to reserves and milk is relatively inefficient at delivering nutrients to offspring. We use dynamic programming to contrast the performance of mothers that provision dependent, refuge-bound offspring optimally from their nutrient reserves with otherwise equivalent mothers that do so directly from the food they find. In this way, we demonstrate formally that the selective advantage to lactating mothers, who can provision--at a cost--without having found food recently, can be substantial with uncertain food supplies and few opportunities for future reproduction under a wide range of circumstances. Hence, it is likely that unreliability associated with the lifestyles of the small, primitive mammal-like reptiles that evolved extended maternal care, selected for fully-developed milk production and consumption, prompting the evolution of true mammals. Moreover, this work suggests that selection for coping with unreliable food access during provisioning may underlie key life-history differences between birds and mammals because the mass constraints imposed by flight restrict the level of reserves that mothers can carry and provision from.

Animal Nutritional Physiological Phenomena↗

Ecological correlates of extra-group paternity in mammals.

Extra-group paternity (EGP) can form an important part of the mating system in birds and mammals. However, our present understanding of its extent and ecology comes primarily from birds. Here, we use data from 26 species and phylogenetic comparative methods to explore interspecific variation in EGP in mammals and test prominent ecological hypotheses for this variation. We found extensive EGP (46% of species showed more than 20% EGP), indicating that EGP is likely to play an important role in the mating system and the dynamics of sexual selection in mammals. Variation in EGP was most closely correlated with the length of the mating season. As the length of the mating season increased, EGP declined, suggesting that it is increasingly difficult for males to monopolize their social mates when mating seasons are short and overlap among females in oestrus is likely to be high. EGP was secondarily correlated with the number of females in a breeding group, consistent with the idea that as female clustering increases, males are less able to monopolize individual females. Finally, EGP was not related to social mating system, suggesting that the opportunities for the extra-group fertilizations and the payoffs involved do not consistently vary with social mating system.

Animals↗

Natural selection at the class II major histocompatibility complex loci of mammals.

The role of natural selection at major histocompatibility complex (MHC) loci was studied by analysis of molecular sequence data from mammalian class II MHC loci. As found previously for the class I MHC molecule and a hypothetical model of the class II molecule, the rate of non-synonymous nucleotide substitution exceeded that of synonymous substitution in the codons encoding the antigen recognition site of polymorphic class II molecules. This pattern is evidence that the polymorphism at these loci is maintained by a form of balancing selection, such as overdominant selection. By contrast, in the case of monomorphic class II loci, no such enhancement of the rate of non-synonymous substitution was observed. Phylogenetic analysis indicates that, in contrast to monomorphic ('non-classical') class I MHC loci, some monomorphic class II loci of mammals are quite ancient. The DMA and DMB loci, for example, diverged before all other known mammalian class II loci, possibly before the divergence of tetrapods from bony fishes. Analysis of the patterns of sharing of polymorphic residues at class II MHC loci by mammals of different species revealed that extensive convergent evolution has occurred at these loci; but no support was found for the hypothesis that MHC polymorphisms have been maintained since before the divergence of orders of eutherian mammals.

Animals↗

Comparative aspects of the inner root sheath in adult and developing hairs of mammals in relation to the evolution of hairs.

The inner root sheath (IRS) allows the exit of hairs through the epidermal surface. The fine structure of monotreme and marsupial IRS and trichohyalin is not known. Using electron microscopy and immunocytochemistry, the localization of trichohyalin and transglutaminase have been studied in monotreme and marsupial hairs, and compared with trichohyalin localization in placental hairs. Trichohyalin in all mammalian species studied here is recognized by a polyclonal antibody against sheep trichohyalin. This generalized immunoreactivity suggests that common epitopes are present in trichohyalin across mammals. In differentiating IRS cells, trichohyalin granules of variable dimensions are composed of an immunolabelled amorphous matrix associated with a network of 10-12-nm-thick keratin filaments. Transglutaminase labelling is present among keratin bundles and trichohyalin granules, and in condensed nuclei of terminally differentiating cells of the inner root sheath. The IRS in monotreme hairs is multistratified but lacks a distinguishable Henle layer. Cornification of IRS determines the sculpturing of the fibre cuticle and later shedding from the follicle for the exit of the hair fibre on the epidermal surface. It is hypothesized that the stratification of IRS in Henle, Huxley and IRS cuticle layers is derived from a simpler organization, like that present in the IRS of monotremes. The IRS is regarded as a localized shedding/sloughing layer needed for the exit of hairs without injury to the epidermis. The formation of the IRS during the evolution of mammalian epidermis allowed the physiological exit of hairs produced inside the skin. The peculiar morphogenesis of hairs in possible primitive skins, such as those of the monotremes (mammals with some reptilian characteristics) or the tails of some rodents (a scaled skin), may elucidate the evolution of hairs. In monotreme and rodent tail skin, the dermal papilla remains localized on the proximal side of the hair peg and forms a hair placode with bilateral symmetry. The papilla is progressively surrounded by the down-growing hair peg until a dermal papilla with radial symmetry is formed. It is speculated that the progressive reduction of the extended dermal papilla of reptilian scales into small and deep papillae of therapsid reptiles produced hairs in mammals.

Animals↗

Vitamin A (retinol and retinyl esters), alpha-tocopherol and lipid levels in plasma of captive wild mammals and birds.

Vitamin A (retinol and retinyl esters), vitamin E and lipids were determined in a wide variety of wild mammals and birds held in captivity. In mammals plasma levels of vitamin A were generally below 500 ng/ml and those of vitamin E were highly variable (0.1-2 micrograms/ml). In primates, vitamin E levels were 3 to 8 micrograms/ml. Whereas in Marsupialia, Chiroptera, primates, Rodentia, Proboscidea, Sirenia, Perissodactyla and Artiodactyla only retinol was found, retinyl esters (basically retinol palmitate/oleate) represented 10 to 50% of the total plasma vitamin A in some birds of the order Ciconiiformes and Falconiformes. Retinol levels in birds were higher compared to mammals (500-2,000 ng/ml). The same was true for lipids as well as for vitamin E levels (1-26 micrograms/ml) in the plasma of birds.

Animals↗

Impacts of roads and hunting on central African rainforest mammals.

Road expansion and associated increases in bunting pressure are a rapidly growing threat to African tropical wildlife. In the rainforests of southern Gabon, we compared abundances of larger (>1 kg) mammal species at varying distances from forest roads and between hunted and unhunted treatments (comparing a 130-km2 oil concession that was almost entirely protected from bunting with nearby areas outside the concession that had moderate hunting pressure). At each of 12 study sites that were evenly divided between hunted and unhunted areas, we established standardized 1-km transects at five distances (50, 300, 600, 900, and 1200 m) from an unpaved road, and then repeatedly surveyed mammals during the 2004 dry and wet seasons. Hunting had the greatest impact on duikers (Cephalophus spp.), forest buffalo (Syncerus caffer nanus), and red river hogs (Potamochoerus porcus), which declined in abundance outside the oil concession, and lesser effects on lowland gorillas (Gorilla gorilla gorilla) and carnivores. Roads depressed abundances of duikers, sitatungas (Tragelaphus spekei gratus), and forest elephants (Loxondonta africana cyclotis), with avoidance of roads being stronger outside than inside the concession. Five monkey species showed little response to roads or hunting, whereas some rodents and pangolins increased in abundance outside the concession, possibly in response to greater forest disturbance. Our findings suggest that even moderate hunting pressure can markedly alter the structure of mammal communities in central Africa. Roads had the greatest impacts on large and small ungulates, with the magnitude of road avoidance increasing with local hunting pressure.

Animals↗

Collaborating to conserve large mammals in Southeast Asia.

Depressed mammal densities characterize the interior of many Southeast Asian protected areas, and are the result of commercial and subsistence hunting. Local people are part of this problem but can participate in solutions through improved partnerships that incorporate local knowledge into problem diagnosis. The process of involving local people helps build a constituency that is more aware of its role (positive and negative) in a protected area and generates site-specific conservation assessments for management planning. We illustrate the practical details of initiating such a partnership through our work in a Thai wildlife sanctuary. Many protected areas in Southeast Asia present similar opportunities. In local workshops, village woodsmen were led through ranking exercises to develop a spatially explicit picture of 20-year trends in the abundance of 31 mammal species and to compare species-specific causes for declines. Within five taxonomic groups, leaf monkeys (primates), porcupines (rodents), tigers (large carnivores), civets (small carnivores), and elephants (ungulates) had declined most severely (37-74%). Commercial hunting contributed heavily to extensive population declines for most species, and subsistence hunting was locally significant for some small carnivores, leaf monkeys, and deer. Workshops thus clarified which species were at highest risk of local extinction, where the most threatened populations were, and causes for these patterns. Most important, they advanced a shared problem definition, thereby unlocking opportunities for collaboration. As a result, local people and sanctuary managers have increased communication, initiated joint monitoring and patrolling, and established wildlife recovery zones. Using local knowledge has limitations, but the process of engaging local people promotes collaborative action that large mammals in Southeast Asia need.

Animals↗

Mitochondrial free radical production and aging in mammals and birds.

The mitochondrial rate of oxygen radical (ROS) production is negatively correlated with maximum life span potential (MLSP) in mammals following the rate of living theory. In order to know if this relationship is more than circumstantial, homeothermic vertebrates with MLSP different from that predicted by the body size and metabolic rate of the majority of mammals (like birds and primates) must be studied. Birds are unique because they combine a high rate of basal oxygen consumption with a high MLSP. Heart, brain, and lung mitochondrial ROS production and free radical leak (percent of total electron flow directed to ROS production) are lower in three species of birds of different orders than in mammals of similar body size and metabolic rate. This suggests that the capacity to show a low rate of ROS production is a general characteristic of birds. Using substrates and inhibitors specific for different segments of the respiratory chain, the main ROS generator site (responsible for those bird-mammalian differences) in state 4 has been localized at complexes I and III in heart mitochondria and only at complex I in nonsynaptic brain mitochondria. In state 3, complex I is the only generator in both tissues. The results also suggest that the iron-sulphur centers are the ROS generators of complex I. A general mechanism that allows pigeon mitochondria to show a low rate of ROS production can be the capacity to maintain a low degree of reduction of the ROS generator site. In heart mitochondria, this is supplemented with a low rate of oxygen consumption physiologically compensated with a comparatively higher heart size. A low rate of free radical production near DNA, together with a high rate of DNA repair, can be responsible for the slow rate of accumulation of DNA damage and thus the slow aging rate of longevous animals.

Aging↗

A software model to estimate zones of impact on marine mammals around anthropogenic noise.

Anthropogenic noise impacts marine mammals in a variety of ways. In order to estimate over which ranges this happens, we first need to understand the propagation of noise through the ocean away from the noise source, and, second, understand the relationship between received noise levels and impact thresholds. A software package combining both aspects is presented. (1) A sound propagation model based on ray theory was developed to calculate received noise levels as a function of range, depth, and frequency. (2) Current knowledge of noise impact thresholds for marine mammals was gathered and included in software routines predicting zones of impact on marine mammals around industrial underwater noise sources. As input parameters, this software package requires the source level and spectrum of the noise of interest; physical oceanography data about the local ocean environment such as bathymetry, bottom and surface loss data, and sound speed profiles; and bioacoustical information about the target species in the form of an audiogram, critical auditory bandwidths, spectra of typical animal vocalizations, reported sound levels of disturbance, and criteria for hearing damage. As output, the software produces data files and plots of the zones of audibility, masking, disturbance, and potential hearing damage around a noise source.

Animals↗

Global mammal conservation: what must we manage?

We present a global conservation analysis for an entire "flagship" taxon, land mammals. A combination of rarity, anthropogenic impacts, and political endemism has put about a quarter of terrestrial mammal species, and a larger fraction of their populations, at risk of extinction. A new global database and complementarity analysis for selecting priority areas for conservation shows that approximately 11% of Earth's land surface should be managed for conservation to preserve at least 10% of terrestrial mammal geographic ranges. Different approaches, from protection (or establishment) of reserves to countryside biogeographic enhancement of human-dominated landscapes, will be required to approach this minimal goal.

Agriculture↗

Quantitative analysis of evolution of the brain in mammals.

Empirical equations derived from brain size (E) and body size (P) of archaic-Eocene, Oligocene, and Recent mammals were all of the form, E = kP(2/3); k = 0.03 for the Eocene, 0.06 for the Oligocene, and 0.12 for the Recent groups. It is suggested that k, which has been used as an index of cephalization in contemporary mammals, may be an appropriate measure of brain evolution in the mammals as a class.

Animals↗

Scaling body support in mammals: limb posture and muscle mechanics.

The scaling of bone and muscle geometry in mammals suggests that peak stresses (ratio of force to cross-sectional area) acting in these two support elements increase with increasing body size. Observations of stresses acting in the limb bones of different sized mammals during strenuous activity, however, indicate that peak bone stress is independent of size (maintaining a safety factor of between 2 and 4). It appears that similar peak bone stresses and muscle stresses in large and small mammals are achieved primarily by a size-dependent change in locomotor limb posture: small animals run with crouched postures, whereas larger species run more upright. By adopting an upright posture, large animals align their limbs more closely with the ground reaction force, substantially reducing the forces that their muscles must exert (proportional to body mass) and hence, the forces that their bones must resist, to counteract joint moments. This change in limb posture to maintain locomotor stresses within safe limits, however, likely limits the maneuverability and accelerative capability of large animals.

Animals↗