Energy assimilation, parental care and the evolution of endothermy

The question of the selection forces which initiated the evolution of endothermy in birds and mammals is one of the most intriguing in the evolutionary physiology of vertebrates. Many students regard the aerobic capacity model as the most plausible hypothesis. This paper presents an alternative model, in which the evolution of endothermy in birds and mammals was driven by two factors: (i) a selection for intense post-hatching parental care, particularly feeding offspring, and (ii) the high cost of maintaining the increased capacity of the visceral organs necessary to support high rates of total daily energy expenditures.     

Parental Care: The Key to Understanding Endothermy and Other Convergent Features in Birds and Mammals

Birds and mammals share a number of features that are remarkably similar but that have evolved independently. One of these characters, endothermy, has been suggested to have played a cardinal role in avian and mammalian evolution. I hypothesize that it is parental care, rather than endothermy, that is the key to understanding the amazing convergence between mammals and birds. Endothermy may have arisen as a consequence of selection for parental care because endothermy enables a parent to control incubation temperature. The remarkable ability of many birds and mammals to sustain vigorous exercise may also have arisen as a consequence of selection for parental care because provisioning of offspring often requires sustained vigorous exercise. Because extensive parental care encompasses a wide range of behaviors, morphology, and physiology, it may be a key innovation that accounts for the majority of convergent avian and mammalian characters.     

Ecology and evolution of extravagant feather ornaments

The ancestral conditions that permit the evolution of extravagant secondary sexual characters are of considerable theoretical and empirical interest because they allow identification of necessary ecological conditions, but also allow empirical tests of models of female mate preferences. We investigated the ancestral and derived state of a range of ecological and evolutionary variables that might have been implicated in the evolution of secondary sexual characters. Extravagant feather ornaments have evolved independently at least 70 times in birds, and the context of these evolutionary events was investigated statistically. The acquisition of feather ornaments was significantly associated with a change in social mating system from monogamy to polygyny or lekking. This association is consistent with the Fisherian mechanism of sexual selection. However, very often also the acquisition of feather ornaments occurred without change in mating system. Therefore, ornamentation can develop for reasons other than polygyny. We did not find any indication of male parental care, kind of food, foraging mode, coloniality, nest site, migration or body mass being significantly associated with a change in the state of ornamentation.     

Evolution of parental care driven by mutual reinforcement of parental food provisioning and sibling competition

In mammals, altricial birds and some invertebrates, parents care for their offspring by providing them with food and protection until independence. Although parental food provisioning is often essential for offspring survival and growth, very little is known about the conditions favouring the evolutionary innovation of this key component of care. Here, we develop a mathematical model for the evolution of parental food provisioning. We find that this evolutionary innovation is favoured when the efficiency of parental food provisioning is high relative to the efficiency of offspring self-feeding and/or parental guarding. We also explore the coevolution between food provisioning and other components of parental care, as well as offspring behaviour. We find that the evolution of food provisioning prompts evolutionary changes in other components of care by allowing parents to choose safer nest sites, and that it promotes the evolution of sibling competition, which in turn further drives the evolution of parental food provisioning. This mutual reinforcement of parental care and sibling competition suggests that evolution of parental food provisioning should show a unidirectional trend from no parental food provisioning to full parental food provisioning.     

Paternity and the evolution of male parental care

It is generally believed that level of paternity (the proportion of zygotes in a brood that were fertilized by the male providing parental care) has an important role in the evolution of parental care. We have used population genetics models to investigate this role. The models indicate that only in mating systems where a parental male “sacrifices” promiscous matings can paternity influence the evolution of male parental care. This is because level of paternity can reflect the number of opportunities for these promiscuous fertilizations. For example, high paternity can mean few opportunities and therefore a low cost for paternal care.Certain behaviors may preadapt a species for the evolution of male parental care because they decrease the costs of providing care. For example, in fish species where male care has evolved from spawning territories, the very establishment of territories may have precluded males from gaining promiscuous matings, thereby eliminating the promiscuity costs and facilitating the evolution of care. Without a promiscuity cost, level of paternity will not have influenced the evolution of male care in fishes.Because paternity has limited influence in the evolution of male care, differences in reliability of parentage between males and females are unlikely to explain the prevalence of female care. Our analysis suggests that paternity differences between species cannot serve as a general explanation for the observed patterns of parental care behavior.     

Repeated parallel evolution of parental care strategies within Xenotilapia, a genus of cichlid fishes from Lake Tanganyika

The factors promoting the evolution of parental care strategies have been extensively studied in experiment and theory. However, most attempts to examine parental care in an evolutionary context have evaluated broad taxonomic categories. The explosive and recent diversifications of East African cichlid fishes offer exceptional opportunities to study the evolution of various life history traits based on species-level phylogenies. The Xenotilapia lineage within the endemic Lake Tanganyika cichlid tribe Ectodini comprises species that display either biparental or maternal only brood care and hence offers a unique opportunity to study the evolution of distinct parental care strategies in a phylogenetic framework. In order to reconstruct the evolutionary relationships among 16 species of this lineage we scored 2,478 Amplified Fragment Length Polymorphisms (AFLPs) across the genome. We find that the Ectodini genus Enantiopus is embedded within the genus Xenotilapia and that during 2.5 to 3 million years of evolution within the Xenotilapia clade there have been 3-5 transitions from maternal only to biparental care. While most previous models suggest that uniparental care (maternal or paternal) arose from biparental care, we conclude from our species-level analysis that the evolution of parental care strategies is not only remarkably fast, but much more labile than previously expected.     

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.     

Social bonds in birds are associated with brain size and contingent on the correlated evolution of life‐history and increased parental investment

In birds, large brains are associated with a series of population‐level phenomena, including invasion success, species richness, and resilience to population decline. Thus, they appear to open up adaptive opportunities through flexibility in foraging and anti‐predator behaviour. The evolutionary pathway leading to large brain size has received less attention than behavioural and ecological correlates. Using a comparative approach, we show that, independent of previously recognized associations with developmental constraints, relative brain size in birds is strongly related to biparental care, pair‐bonding, and stable social relationships. We also demonstrate correlated evolution between large relative brain size and altricial development, and that the evolution of both traits is contingent on biparental care. Thus, biparental care facilitates altricial development, which permits the evolution of large relative brain size. Finally, we show that large relative brain size is associated with pair‐bond strength, itself a likely consequence of cooperation and negotiation between partners under high levels of parental investment. These analyses provide an evolutionary model for the evolution of and prevalence of biparental care, altricial development, and pair‐bonding in birds. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 111–123.     

Clutch size evolution under sexual conflict enhances the stability of mating systems.

Models of optimal clutch size often implicitly assume a situation with uniparental care. However, the evolutionary conflict between males and females over the division of parental care will have a major influence on the evolution of clutch size. Since clutch size is a female trait, a male has little possibility of directly influencing it. However, the optimal clutch size from a female's perspective will depend on the amount of paternal care her mate is expected to provide. The sexual conflict over parental care will in its turn be affected by clutch size, since a larger clutch makes male care more valuable. Hence, there will be joint evolution of mating system and clutch size. In this paper, we demonstrate that this joint evolution will tend to stabilize the mating system. In a situation with conventional sex roles, this joint evolution might result in either increased clutch size and biparental care or reduced clutch size and uniparental female care. Under some circumstances the initial conditions might determine which will be the outcome. These results demonstrate that it may be difficult to deduce whether biparental care evolved because of few opportunities for breeding males increasing their fitness by attracting additional mates or because of the importance of male care for offspring fitness by studying prevailing mating systems using, for example, male removals or manipulation of males' opportunities for finding additional mates. In general terms, we demonstrate that models of life-history evolution have to consider the social context in which they evolve.     

The other facets of family life and their role in the evolution of animal sociality

Family life forms an integral part of the life history of species across the animal kingdom and plays a crucial role in the evolution of animal sociality. Our current understanding of family life, however, is almost exclusively based on studies that (i) focus on parental care and associated family interactions (such as those arising from sibling rivalry and parent‐offspring conflict), and (ii) investigate these phenomena in the advanced family systems of mammals, birds, and eusocial insects. Here, we argue that these historical biases have fostered the neglect of key processes shaping social life in ancestral family systems, and thus profoundly hamper our understanding of the (early) evolution of family life. Based on a comprehensive survey of the literature, we first illustrate that the strong focus on parental care in advanced social systems has deflected scrutiny of other important social processes such as sibling cooperation, parent–offspring competition and offspring assistance. We then show that accounting for these neglected processes – and their changing role over time – could profoundly alter our understanding of the origin and subsequent evolution of family life. Finally, we outline how this ‘diachronic’ perspective on the evolution of family living provides novel insights into general processes driving the evolution of animal sociality. Overall, we infer that the explicit consideration of thus‐far neglected facets of family life, together with their study across the whole diversity of family systems, are crucial to advance our understanding of the processes that shape the evolution of social life.     

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.     

Hibernation is associated with increased survival and the evolution of slow life histories among mammals

Survival probability is predicted to underlie the evolution of life histories along a slow-fast continuum. Hibernation allows a diverse range of small mammals to exhibit seasonal dormancy, which might increase survival and consequently be associated with relatively slow life histories. We used phylogenetically informed GLS models to test for an effect of hibernation on seasonal and annual survival, and on key attributes of life histories among mammals. Monthly survival was in most cases higher during hibernation compared with the active season, probably because inactivity minimizes predation. Hibernators also have approximately 15 per cent higher annual survival than similar sized non-hibernating species. As predicted, we found an effect of hibernation on the relationships between life history attributes and body mass: small hibernating mammals generally have longer maximum life spans (50% greater for a 50 g species), reproduce at slower rates, mature at older ages and have longer generation times compared with similar-sized non-hibernators. In accordance with evolutionary theories, however, hibernating species do not have longer life spans than non-hibernators with similar survival rates, nor do they have lower reproductive rates than non-hibernators with similar maximum life spans. Thus, our combined results suggest that (i) hibernation is associated with high rates of overwinter and annual survival, and (ii) an increase in survival in hibernating species is linked with the coevolution of traits indicative of relatively slow life histories.     

Phylogenetic perspectives in the evolution of parental care in ray-finned fishes

Among major vertebrate groups, ray-finned fishes (Actinopterygii) collectively display a nearly unrivaled diversity of parental care activities. This fact, coupled with a growing body of phylogenetic data for Actinopterygii, makes these fishes a logical model system for analyzing the evolutionary histories of alternative parental care modes and associated reproductive behaviors. From an extensive literature review, we constructed a supertree for ray-finned fishes and used its phylogenetic topology to investigate the evolution of several key reproductive states including type of parental care (maternal, paternal, or biparental), internal versus external fertilization, internal versus external gestation, nest construction behavior, and presence versus absence of sexual dichromatism (as an indicator of sexual selection). Using a comparative phylogenetic approach, we critically evaluate several hypotheses regarding evolutionary pathways toward parental care. Results from maximum parsimony reconstructions indicate that all forms of parental care, including paternal, biparental, and maternal (both external and internal to the female reproductive tract) have arisen repeatedly and independently during ray-finned fish evolution. The most common evolutionary transitions were from external fertilization directly to paternal care and from external fertilization to maternal care via the intermediate step of internal fertilization. We also used maximum likelihood phylogenetic methods to test for statistical correlations and contingencies in the evolution of pairs of reproductive traits. Sexual dichromatism and nest construction proved to be positively correlated with the evolution of male parental care in species with external fertilization. Sexual dichromatism was also positively correlated with female-internal fertilization and gestation. No clear indication emerged that female-only care or biparental care were evolutionary outgrowths of male-only care, or that biparental care has been a common evolutionary stepping stone between paternal and maternal care. Results are discussed in the context of prior thought about the evolution of alternative parental care modes in vertebrates.     

The evolution of coloniality: the emergence of new perspectives

The evolution of group living remains an outstanding question in evolutionary ecology. Among the most striking forms of group living are the enormous assemblages of breeders that occur in many colonial marine birds and mammals, with some colonies containing more than a million individuals breeding in close contact. Coloniality is an evolutionary puzzle because individuals pay fitness costs to breed in high densities. Despite numerous potential benefits proposed to overcome these costs, we still lack a general framework to explain coloniality. Several new hypotheses involving breeding habitat and mate selection create promising approaches for studying this enigma.     

Speciation and extinction drive the appearance of directional range size evolution in phylogenies and the fossil record

While the geographic range of a species is a fundamental unit of macroecology and a leading predictor of extinction risk, the evolutionary dynamics of species' ranges remain poorly understood. Based on statistical associations between range size and species age, many studies have claimed support for general models of range evolution in which the area occupied by a species varies predictably over the course of its life. Such claims have been made using both paleontological data and molecular estimates of the age of extant species. However, using a stochastic model, we show that the appearance of trends in range size with species' age can arise even when range sizes have evolved at random through time. This occurs because the samples of species used in existing studies are likely to be biased with respect to range size: for example, only those species that happened to have large or expanding ranges are likely to survive to the present, while extinct species will tend to be those whose ranges, by chance, declined through time. We compared the relationship between the age and range size of species arising under our stochastic model to those observed across 1,269 species of extant birds and mammals and 140 species of extinct Cenozoic marine mollusks. We find that the stochastic model is able to generate the full spectrum of empirical age-area relationships, implying that such trends cannot be simply interpreted as evidence for models of directional range size evolution. Our results therefore challenge the theory that species undergo predictable phases of geographic expansion and contraction through time.     

The evolution and diversification of sleep

The evolutionary origins of sleep and its sub-states, rapid eye movement (REM) and non-REM (NREM) sleep, found in mammals and birds, remain a mystery. Although the discovery of a single type of sleep in jellyfish suggests that sleep evolved much earlier than previously thought, it is unclear when and why sleep diversified into multiple types of sleep. Intriguingly, multiple types of sleep have recently been found in animals ranging from non-avian reptiles to arthropods to cephalopods. Although there are similarities between these states and those found in mammals and birds, notable differences also exist. The diversity in the way sleep is expressed confounds attempts to trace the evolution of sleep states, but also serves as a rich resource for exploring the functions of sleep.     

The evolution of parental care in insects: the roles of ecology,life history and the social environment

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Climate change and size evolution in an island rodent species: new perspectives on the island rule

As stated by the island rule, small mammals evolve toward gigantism on islands. In addition they are known to evolve faster than their mainland counterparts. Body size in island mammals may also be influenced by geographical climatic gradients or climatic change through time. We tested the relative effects of climate change and isolation on the size of the Japanese rodent Apodemus speciosus and calculated evolutionary rates of body size change since the last glacial maximum (LGM). Currently A. speciosus populations conform both to Bergmann's rule, with an increase in body size with latitude, and to the island rule, with larger body sizes on small islands. We also found that fossil representatives of A. speciosus are larger than their extant relatives. Our estimated evolutionary rates since the LGM show that body size evolution on the smaller islands has been less than half as rapid as on Honshu, the mainland-type large island of Japan. We conclude that island populations exhibit larger body sizes today not because they have evolved toward gigantism, but because their evolution toward a smaller size, due to climate warming since the LGM, has been decelerated by the island effect. These combined results suggest that evolution in Quaternary island small mammals may not have been as fast as expected by the island effect because of the counteracting effect of climate change during this period.     

The evolution of parental care and egg size: a comparative analysis in frogs

The evolution of parental care and egg size has attracted considerable attention and theoretical debate. Several different hypotheses have been proposed concerning the trajectories of parental care and egg size evolution and the order of specific evolutionary transitions. Few comparative studies have investigated the predictions of these hypotheses. Here, we investigate the evolutionary association between parental care and egg size in frogs in a phylogenetic context. Data on egg size and presence or absence of parental care in various species of frogs was gathered from the scientific literature. As a basis for our comparative analyses, we developed a phylogenetic supertree, by combining the results of multiple phylogenetic analyses in the literature using matrix representation parsimony. Using phylogenetic pairwise comparisons we demonstrated a significant association between the evolution of parental care and large egg size. We then used recently developed maximum likelihood methods to infer the evolutionary order of specific transitions. This analysis revealed that the evolution of large egg size typically precedes the evolution of parental care, rather than the reverse. We discuss the relevance of our results to previous hypotheses concerning the evolution of parental care and egg size.     

The evolution of parental care in insects: A test of current hypotheses

Which sex should care for offspring is a fundamental question in evolution. Invertebrates, and insects in particular, show some of the most diverse kinds of parental care of all animals, but to date there has been no broad comparative study of the evolution of parental care in this group. Here, we test existing hypotheses of insect parental care evolution using a literature‐compiled phylogeny of over 2000 species. To address substantial uncertainty in the insect phylogeny, we use a brute force approach based on multiple random resolutions of uncertain nodes. The main transitions were between no care (the probable ancestral state) and female care. Male care evolved exclusively from no care, supporting models where mating opportunity costs for caring males are reduced—for example, by caring for multiple broods—but rejecting the “enhanced fecundity” hypothesis that male care is favored because it allows females to avoid care costs. Biparental care largely arose by males joining caring females, and was more labile in Holometabola than in Hemimetabola. Insect care evolution most closely resembled amphibian care in general trajectory. Integrating these findings with the wealth of life history and ecological data in insects will allow testing of a rich vein of existing hypotheses.