The molecular evolution of ZFY-related genes in birds and mammals

Summary We report the isolation and nucleotide sequence determination of clones derived from five ZFY-related zinc-finger genes from birds and mammals. These sequences are analyzed with reference to the previously published human genes, ZFX and ZFY, and mouse genes, Zfx, Zfa, Zfy-1, and Zfy-2. The analysis indicates that ZFY-related genes are highly conserved in birds and mammals, and that the rate of nucleotide substitution in the Y-linked genes is not as high as predicted. However, the mouse Zfy-1 and Zfy-2 genes are markedly divergent members of the ZFY gene family; we suggest this relates to X-inactivation of the mouse gene Zfx.     

Diversity and evolution of T-cell receptor variable region genes in mammals and birds

 The receptor of a T lymphocyte (TCR) recognizes nonself antigens in the company of major histocompatibility complex (MHC) molecules presented to it by the antigen-presenting cell. The variable region of TCR is encoded by either a concatenation of variable region (TCR-V), diversity region (TCR-D), and joining region (TCR-J) genes, or a concatenation of TCR-V and TCR-J genes. The TCR-V genes exist as a multigene family in vertebrate species. Here we study the evolutionary relationships of TCR-V genes from humans, sheep, cattle, rabbits, mice, and chicken. These six species can be classified into two groups according to the frequency of γδ T-cells in their peripheral T-cell populations. The "γδ low" group of species includes humans and mice, in which γδ T-cells constitute very limited portion of the T-cell population. The "γδ high" group includes sheep, cattle, rabbits, and chicken, in which γδ T-cells comprise up to 60% of the T-cell population. Here, we compiled TCR-V sequences from the six species and conducted a phylogenetic analysis. We identified various TCR-V gene subgroups based on the analysis. We found that humans and mice have representatives from nearly all of the subgroups identified, while other species have lost subgroups to different extent. Therefore, the γδ low species have a high degree of diversity of TCR-V genes, while γδ high species all have limited diversity of TCR-V genes. This pattern is similar to that found for immunoglobulin variable region (IGV) genes. Received: 20 May 1999 / Revised: 13 July 1999     

Construction and evolution of imprinted loci in mammals

Genomic imprinting first evolved in mammals around the time that humans last shared a common ancestor with marsupials and monotremes (180-210 million years ago). Recent comparisons of large imprinted domains in these divergent mammalian groups have shown that imprinting evolved haphazardly at various times in different lineages, perhaps driven by different selective forces. Surprisingly, some imprinted domains were formed relatively recently, using non-imprinted components acquired from unexpected genomic regions. Rearrangement and the insertion of retrogenes, small nucleolar RNAs, microRNAs, differential CpG methylation and control by non-coding RNA often accompanied the acquisition of imprinting. Here, we use comparisons between different mammalian groups to chart the course of evolution of two related epigenetic regulatory systems in mammals: genomic imprinting and X-chromosome inactivation.     

Rates of evolution of hybrid inviability in birds and mammals

Almost 30 years ago, A. C. Wilson and colleagues presented results indicating that hybrid inviability between species evolves 10 times faster in mammals than in birds and frogs. Here I revisit this question for birds and mammals using modern molecular data (mitochondrial cytochrome b DNA) and a more phylogenetically appropriate statistical approach. My analyses confirm that diverging mammals lose the ability to form viable hybrids faster than birds. To explain the difference in rates of evolutionary loss of hybridization potential, Wilson and coworkers proposed that mammals have higher rates of regulatory evolution, causing higher probabilities of developmental incompatibilities between mammal species. I briefly discuss this and other potential explanations.     

The evolution of concepts on the evolution of endothermy in birds and mammals

Warm-blooded animals, mammals and birds, are unique not because they are endothermic in the strict sense of the term but because they use an extravagant economy: they have high energy budgets and spend a large part of their energy resources on basic maintenance. Although several advantages of endothermy are easy to indicate, mechanisms behind evolution of such a wasteful life strategy remain unclear and have been subject to intensive debate. For two decades, the aerobic capacity model has been widely recognized as a promising hypothesis and has catalyzed a new direction in ecological and evolutionary physiology--the study of correlated evolution of behavioral and morphophysiological traits. Recently, two alternative models have been proposed, both of which see evolution of high metabolic rates in birds and mammals as an element in evolution of intensive parental care. Unlike previous models, which treated individuals as static objects of fixed properties, the parental care models explicitly incorporate life histories into a evolutionary-physiology research program. The aim of this article was to outline the process of evolution of major concepts in the field, which reflects development of the paradigm of modern evolutionary physiology.     

The evolution of endothermy and its diversity in mammals and birds

Many elements of mammalian and avian thermoregulatory mechanisms are present in reptiles, and the changes involved in the transition to endothermy are more quantitative than qualitative. Drawing on our experience with reptiles and echidnas, we comment on that transition and on current theories about how it occurred. The theories divide into two categories, depending on whether selection pressures operated directly or indirectly on mechanisms producing heat. Both categories of theories focus on explaining the evolution of homeothermic endothermy but ignore heterothermy. However, noting that hibernation and torpor are almost certainly plesiomorphic (=ancestral, primitive), and that heterothermy is very common among endotherms, we propose that homeothermic endothermy evolved via heterothermy, with the earliest protoendotherms being facultatively endothermic and retaining their ectothermic capacity for "constitutional eurythermy." Thus, unlike current models for the evolution of endothermy that assume that hibernation and torpor are specialisations arising from homeothermic ancestry, and therefore irrelevant, we consider that they are central. We note the sophistication of thermoregulatory behavior and control in reptiles, including precise control over conductance, and argue that brooding endothermy seen in some otherwise ectothermic Boidae suggests an incipient capacity for facultative endothermy in reptiles. We suggest that the earliest insulation in protoendotherms may have been internal, arising from redistribution of the fat bodies that are typical of reptiles. We note that short-beaked echidnas provide a useful living model of what an (advanced) protoendotherm may have been like. Echidnas have the advantages of endothermy, including the capacity for homeothermic endothermy during incubation, but are very relaxed in their thermoregulatory precision and minimise energetic costs by using ectothermy facultatively when entering short- or long-term torpor. They also have a substantial layer of internal dorsal insulation. We favor theories about the evolution of endothermy that invoke direct selection for the benefits conferred by warmth, such as expanding daily activity into the night, higher capacities for sustained activity, higher digestion rates, climatic range expansion, and, not unrelated, control over incubation temperature and the benefits for parental care. We present an indicative, stepwise schema in which observed patterns of body temperature are a consequence of selection pressures, the underlying mechanisms, and energy optimization, and in which homeothermy results when it is energetically desirable rather than as the logical endpoint.     

A phenology of the evolution of endothermy in birds and mammals

Recent palaeontological data and novel physiological hypotheses now allow a timescaled reconstruction of the evolution of endothermy in birds and mammals. A three‐phase iterative model describing how endothermy evolved from Permian ectothermic ancestors is presented. In Phase One I propose that the elevation of endothermy – increased metabolism and body temperature (T_b) – complemented large‐body‐size homeothermy during the Permian and Triassic in response to the fitness benefits of enhanced embryo development (parental care) and the activity demands of conquering dry land. I propose that Phase Two commenced in the Late Triassic and Jurassic and was marked by extreme body‐size miniaturization, the evolution of enhanced body insulation (fur and feathers), increased brain size, thermoregulatory control, and increased ecomorphological diversity. I suggest that Phase Three occurred during the Cretaceous and Cenozoic and involved endothermic pulses associated with the evolution of muscle‐powered flapping flight in birds, terrestrial cursoriality in mammals, and climate adaptation in response to Late Cenozoic cooling in both birds and mammals. Although the triphasic model argues for an iterative evolution of endothermy in pulses throughout the Mesozoic and Cenozoic, it is also argued that endothermy was potentially abandoned at any time that a bird or mammal did not rely upon its thermal benefits for parental care or breeding success. The abandonment would have taken the form of either hibernation or daily torpor as observed in extant endotherms. Thus torpor and hibernation are argued to be as ancient as the origins of endothermy itself, a plesiomorphic characteristic observed today in many small birds and mammals.     

Insights into the evolution of mammalian telomerase: Platypus TERT shares similarities with genes of birds and other reptiles and localizes on sex chromosomes

ABSTRACT: BACKGROUND: The TERT gene encodes the catalytic subunit of the telomerase complex and is responsible for maintaining telomere length. Vertebrate telomerase has been studied in placental mammals, fish, and the chicken, but less attention has been paid to other vertebrates. The platypus occupies an important evolutionary position, providing unique insight into the evolution of mammalian genes. We report the cloning of a platypus TERT (pTERT) ortholog, and provide a comparison with genes of other vertebrates. RESULTS: The pTERT encodes a protein with the high homology to marsupial TERT and avian TERT. Like the TERT of sauropsids and marsupials, as well as that of sharks and echinoderms, pTERT contains extended variable linkers in the N-terminal region suggesting that they were present already in basal vertebrates and lost independently in placental mammals and ray-finned fish. Several alternatively spliced pTERT variants structurally similar to avian TERT variants were identified. Telomerase activity is expressed in all platypus tissues similarly to cold-blooded animals and murine rodents. pTERT was localized on pseudoautosomal regions of sex chromosomes X3/Y2, expanding the homology between human chromosome 5 and platypus sex chromosomes. The synteny analysis suggests that TERT co-localized with sex-linked genes in the last common mammalian ancestor. Interestingly, female platypuses express higher levels of telomerase in heart and liver tissues than do males. CONCLUSIONS: pTERT shares many features with TERT of the reptilian outgroup, suggesting that pTERT represents the ancestral mammalian TERT. Features specific to TERT of eutherian mammals have, therefore, evolved more recently after the divergence of monotremes.     

Nucleotide sequence analysis of the lemur beta-globin gene family: evidence for major rate fluctuations in globin polypeptide evolution

Lemur beta-related globin genes have been isolated and sequenced. Orthology of prosimian and human epsilon-, gamma-, and beta-related globin genes was established by dot-matrix analysis. All of these lemur globin genes potentially encode functional beta-related globin polypeptides, though precisely when the gamma-globin gene is expressed remains unknown. The organization of the 18-kb brown lemur beta-globin gene cluster (5' epsilon-gamma-[psi eta-delta]-beta 3') is consistent with its evolution by contraction via unequal crossing-over from the putative ancestral mammalian beta-globin gene cluster (5' epsilon-gamma- eta-delta-beta 3'). The dwarf lemur nonadult globin genes are arranged as in the brown lemur. Similar levels of synonymous (silent) nucleotide substitutions and noncoding DNA sequence differences have accumulated between species in all of these genes, suggesting a uniform rate of noncoding DNA divergence throughout primate beta-globin gene clusters. These differences are comparable with those observed in the nonfunctional psi eta pseudogene and have therefore accumulated at the presumably maximal neutral rate. In contrast, nonsynonymous (replacement) nucleotide substitutions show a significant heterogeneity in distribution for both the same gene in different lineages and different genes in the same lineage. These major fluctuations in replacement but not silent substitution rates cannot be attributed to changes in mutation rate, suggesting that changes in the rate of globin polypeptide evolution in primates is not governed solely by variable mutation rates.      

Independent evolution of Toll and related genes in insects and mammals

 Toll and Toll-related proteins play an important role in antibacterial innate immunity in insect, plants, and mammals. We present the first comprehensive phylogenetic analyses of Toll-related genes from both insects and mammals. Drosophila melanogaster contains Toll and a highly homologous gene, Tehao. The protein, Dm Tehao, comprises 795 amino acid residues and its cytoplasmic domain shares a striking 61% identity with Dm Toll. Two Toll homologues were found in another dipteran of medical importance, Anopheles gambiae, a vector for human malaria. One Toll-like gene each was identified from Aedes aegypti and Glossina palpalis palpalis, vectors for yellow fever and trypanosomiasis, respectively. Phylogenetic analyses revealed separate clustering of Toll and related proteins from insects and mammals, suggesting independent evolution of the Toll family of proteins and of innate immunity in arthropods and vertebrates. These results also provide new avenues to understanding the function of Toll proteins in insect innate immunity against bacteria, fungi, and protozoans. Received: 25 June 1999 / Revised: 25 September 1999     

Heterothermy in Afrotropical mammals and birds: a review

Recent years have seen a rapid increase in the number of Afrotropical endotherms known to avoid mismatches between energy supply and demand by using daily torpor and/or hibernation. Among mammals, heterothermy has been reported in 40 species in six orders, namely Macroscelidea, Afrosoricida, Rodentia, Eulipotyphla, Primates and Chiroptera. These species span a range in body mass of 7-770?g, with minimum heterothermic body temperatures ranging from 1-27°C and bout length varying from 1?h to 70 days. Daily torpor is the most common form of heterothermy, with true hibernation being observed in only seven species, Graphiurus murinus, Graphiurus ocularis, Atelerix frontalis, Cheirogaleus medius, Cheirogaleus major, Microcebus murinus and Microcebus griseorufus. The traditional distinction between daily torpor and hibernation is blurred in some species, with free-ranging individuals exhibiting bouts of > 24?h and body temperatures < 16 °C, but none of the classical behaviours associated with hibernation. Several species bask in the sun during rewarming. Among birds, heterothermy has been reported in 16 species in seven orders, and is more pronounced in phylogenetically older taxa. Both in mammals and birds, patterns of heterothermy can vary dramatically among species occurring at a particular site, and even among individuals of a single species. For instance, patterns of heterothermy among cheirogalid primates in western Madagascar vary from daily torpor to uninterrupted hibernation for up to seven months. Other examples of variation among closely-related species involve small owls, elephant shrews and vespertilionid bats. There may also be variation in terms of the ecological correlates of torpor within a species, as is the case in the Freckled Nightjar Caprimulgus tristigma.     

Coalescent analyses of multiple loci support a new route to speciation in birds

A widely accepted paradigm is that sedentary Neotropical bird species are a reservoir that gives rise to temperate-tropical migratory species. Recently, an alternative theory has been proposed, that developmental plasticity can allow some individuals within a migratory species to establish a disjunct breeding range through loss of migration, thus facilitating the founding of a new sedentary species. We used mtDNA and two nuclear introns to perform coalescent analyses for two closely related New World oriole species, one a long-distance temperate-tropical migrant and the other a short-distance intratropical migrant. Our results suggest that the short-distance migrant recently diverged from the long-distance migrant via a founder event. In this species pair, the widely accepted paradigm is not supported. These results are consistent with a model of speciation through reduction of migratory distance.     

Scaling of organ subunits in adult mammals and birds: A model

Members of one class of organs—including kidney and lung—consist chiefly of repeating units, or subunits, similar in size and shape. Across species, both the number and size of repeating units may increase with increasing organ size. A simple model is proposed, relating the scaling of unit-size and unit-number to that of organ volume. The model makes three structural assumptions, the crucial one, biologically speaking, being that the numerical density of repeating units scales as does organ surface-to-volume ratio. Data were collected from the literature bearing on the number, diameter, total surface area and total volume of such repeating units (i.e., alveoli, air capillaries, renal tubules and glomeruli), for avian and mammalian lung and for mammalian kidney, each as a function of organ size. These data, after log-log transformation, were submitted to standard linear least squares regression analysis. The resultant slopes for nine different regression lines are in good agreement with the model predictions. This finding suggests, surprisingly, that organ scale-up, at least for selected organs, expressed in terms of repeating units, as a function of organ volume, in mammals and birds, and conceivably in other phyla, may be based on a small number of elementary structural principles.     

Impact of carnivory on human development and evolution revealed by a new unifying model of weaning in mammals

Our large brain, long life span and high fertility are key elements of human evolutionary success and are often thought to have evolved in interplay with tool use, carnivory and hunting. However, the specific impact of carnivory on human evolution, life history and development remains controversial. Here we show in quantitative terms that dietary profile is a key factor influencing time to weaning across a wide taxonomic range of mammals, including humans. In a model encompassing a total of 67 species and genera from 12 mammalian orders, adult brain mass and two dichotomous variables reflecting species differences regarding limb biomechanics and dietary profile, accounted for 75.5%, 10.3% and 3.4% of variance in time to weaning, respectively, together capturing 89.2% of total variance. Crucially, carnivory predicted the time point of early weaning in humans with remarkable precision, yielding a prediction error of less than 5% with a sample of forty-six human natural fertility societies as reference. Hence, carnivory appears to provide both a necessary and sufficient explanation as to why humans wean so much earlier than the great apes. While early weaning is regarded as essentially differentiating the genus Homo from the great apes, its timing seems to be determined by the same limited set of factors in humans as in mammals in general, despite some 90 million years of evolution. Our analysis emphasizes the high degree of similarity of relative time scales in mammalian development and life history across 67 genera from 12 mammalian orders and shows that the impact of carnivory on time to weaning in humans is quantifiable, and critical. Since early weaning yields shorter interbirth intervals and higher rates of reproduction, with profound effects on population dynamics, our findings highlight the emergence of carnivory as a process fundamentally determining human evolution.     

Topology and maturation of filamentous haemagglutinin suggest a new model for two-partner secretion

Two-partner secretion (TPS) is the most widely distributed secretion pathway known. These systems export large exoproteins through highly conserved channel-forming beta-barrel proteins. Filamentous haemagglutinin (FHA), expressed by Bordetella species, is the prototypical TPS family member. Here we show that the C-terminus of mature FHA, as opposed to the N-terminus as previously proposed, is exposed on the cell surface and is required for mediating adherence to cultured epithelial cells. We show that the C-terminus of the FHA pro-protein (FhaB) is required for FHA function in vitro and in vivo and we show that cleavage of FhaB to form FHA is not the mechanism by which FHA is released from the cell. Based on these data, we propose a new model for TPS. This model provides an explanation for the energetics of export of globular protein domains across membranes in the absence of ATP and it suggests a new mechanism for the control of protein folding.     

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.     

Hypothalamic expression of thyroid hormone-activating and -inactivating enzyme genes in relation to photorefractoriness in birds and mammals

Photorefractoriness is the insensitivity of gonadal development to the stimulatory effects of long photoperiods in birds and to the inhibitory effects of short photoperiods in small mammals. Its molecular mechanism remains unknown. Recently, it has been shown that reciprocal expression of thyroid hormone-activating enzyme [type 2 deiodinase (Dio2)] and -inactivating enzyme [type 3 deiodinase (Dio3)] genes in the mediobasal hypothalamus is critical for photoperiodically induced gonadal growth. Since thyroid hormones are required not only for photoinduction, but also for the induction of photorefractoriness, we examined the expression of these genes in relation to photorefractoriness in birds and mammals. Transfer of birds to long photoperiods induced strong expression of Dio2. This was maintained in tree sparrow when they later became photorefractory, but decreased somewhat in quail. In hamsters, transfer to long photoperiods also induced strong expression of Dio2. High values were not maintained under long photoperiods, and, indeed, expression decreased at the same rate as in animals transferred to short photoperiods. There was no renewed expression of Dio2 associated with testicular growth as animals became refractory to short photoperiods. Expression of Dio3 was high under short photoperiods and low under long photoperiods in all the animals examined, except for the short photoperiod-refractory hamsters. Our present study revealed complex regulation of deiodinase genes in the photoinduction and photorefractory processes in birds and mammals. These gene changes may be involved in the regulation of photorefractoriness, as well as photoinduction.     

Climate variability and the energetic pathways of evolution: the origin of endothermy in mammals and birds

Large-scale climate oscillations in earth's history have influenced the directions of evolution, last but not least, through mass extinction events. This analysis tries to identify some unifying forces behind the course of evolution that favored an increase in organismic complexity and performance, paralleled by an increase in energy turnover, and finally led to endothermy. The analysis builds on the recent concept of oxygen-limited thermal tolerance and on the hypothesis that unifying principles exist in the temperature-dependent biochemical design of the eukaryotic cell in animals. The comparison of extant water-breathing and air-breathing animal species from various climates provides a cause-and-effect understanding of the trade-offs and constraints in thermal adaptation and their energetic consequences. It is hypothesized that the high costs of functional adaptation to fluctuating temperatures, especially in the cold (cold eurythermy), cause an increase in energy turnover and, at the same time, mobility and agility. These costs are associated with elevated mitochondrial capacities at minimized levels of activation enthalpies for proton leakage. Cold eurythermy is seen as a precondition for the survival of evolutionary crises elicited by repeated cooling events during extreme climate fluctuations. The costs of cold eurythermy appear as the single most important reason why metazoan evolution led to life forms with high energy turnover. They also explain why dinosaurs were able to live in subpolar climates. Finally, they give insight into the pathways, benefits, and trade-offs involved in the evolution of constant, elevated body temperature maintained by endothermy. Eurythermy, which encompasses cold tolerance, is thus hypothesized to be the "missing link" between ectothermy and endothermy. Body temperatures between 32 degrees and 42 degrees C in mammals and birds then result from trade-offs between the limiting capacities of ventilation and circulation and the evolutionary trend to maximize performance at the warm end of the thermal tolerance window.