The evolution of body size in birds. I. Evidence for non-random diversification

The hypothesis that evolution of body size in birds was a random process coupled with an absolute lower boundary on body mass was tested using data on 6217 species of extant birds. The test was based on the fact that subclades within birds that have body masses much larger than this minimum should not have skewed log body mass distributions, while clades close to this boundary should. Bird species were classified into 23 orders suggested by Sibley and Monroe (1988). Thirteen orders that had average log body masses greater than the average for all birds had significantly skewed log body mass distributions. This is inconsistent with the hypothesis that evolution of body size in birds is random, but is constrained only at the smallest body masses. Most orders of birds cannot be considered random samples from the parental distribution of all birds. When the pattern of body mass evolution in birds is reconstructed using an estimate of the phylogenetic relationships among orders, there are many more instances where a large taxon putatively originated from a smaller one than vice versa. The non-random nature of body mass evolution in birds is consistent with models that postulate that evolution is constrained by the ability of individuals to turn resources into offspring.     

Body size evolution in Mesozoic birds

The tendency for the mean body size of taxa within a clade to increase through evolution (Cope's Rule) has been demonstrated in a number of terrestrial vertebrate groups. However, because avian body size is strongly constrained by flight, any increase in size during the evolution of this lineage should be limited - there is a maximum size that can be attained by a bird for it to be able to get off the ground. Contrary to previous interpretations of early avian evolution, we demonstrate an overall increase in body size across Jurassic and Cretaceous flying birds: taxon body size increases from the earliest Jurassic through to the end of the Cretaceous, across a time span of 70 Myr. Although evidence is limited that this change is directional, it is certainly nonrandom. Relative size increase occurred presumably as the result of an increase in variance as the avian clade diversified after the origin of flight: a progression towards larger body size is seen clearly within the clades Pygostylia and Ornithothoraces. In contrast, a decrease in body size characterizes the most crownward lineage Ornithuromorpha, the clade that includes all extant taxa, and potentially may explain the survival of these birds across the Cretaceous-Palaeogene boundary. As in all other dinosaurs, counter selection for small size is seen in some clades, whereas body size is increasing overall.     

The evolution of parental care in freshwater leeches

Summary The life-history strategies of a selection of the most common European freshwater leeches (Euhirudinea) are described. On the basis of this information and results from the literature, the probable phylogenetic development of parental care in the Euhirudinea is reconstructed. The jawless worm leeches (Erpobdellidae) secrete a protective cocoon, cement it to the substrate and sometimes ventilate it before they leave the egg capsules. This behaviour represents the most ancient state in leech evolution. Members of the jawed Hirudinidae deposit desiccation-resistant cocoons on land. All known Glossiphoniidae (leeches equipped with a proboscis) have evolved the habit of brooding the eggs and young. These unique parental care patterns within one family of extant freshwater leeches can be arranged schematically in a series of increasing complexity which may reflect the evolution of brooding behaviour. Glossiphoniid leeches of the genus Helobdella, which have a world-wide distribution, display the most highly developed parental care system: they not only protect but also feed the young they carry. This results in the young being much larger when they leave the parent and, presumably, in higher subsequent survival. Isolated cocoons of all aquatic leeches are rapidly destroyed by predators, primarily water snails. In erpobdellids (but not glossiphoniids, which protect the cocoons) a large portion of the cocoons are lost due to predatory attacks. We conclude that the major selective pressure driving the evolution of parental care in leeches may have been predation on eggs and juvenile stages. Dedicated to Professor Dr. G. Osche on the occasion of his 75th birthday     

Body size evolution in Mesozoic birds: little evidence for Cope's rule

Cope's rule, the tendency towards evolutionary increases in body size, is a long-standing macroevolutionary generalization that has the potential to provide insights into directionality in evolution; however, both the definition and identification of Cope's rule are controversial and problematic. A recent study [J. Evol. Biol. 21 (2008) 618] examined body size evolution in Mesozoic birds, and claimed to have identified evidence of Cope's rule occurring as a result of among-lineage species sorting. We here reassess the results of this study, and additionally carry out novel analyses testing for within-lineage patterns in body size evolution in Mesozoic birds. We demonstrate that the nonphylogenetic methods used by this previous study cannot distinguish between among- and within-lineage processes, and that statistical support for their results and conclusions is extremely weak. Our ancestor-descendant within-lineage analyses explicitly incorporate recent phylogenetic hypotheses and find little compelling evidence for Cope's rule. Cope's rule is not supported in Mesozoic birds by the available data, and body size evolution currently provides no insights into avian survivorship through the Cretaceous-Paleogene mass extinction.     

Toward a synthetic understanding of the role of phenology in ecology and evolution

Phenology affects nearly all aspects of ecology and evolution. Virtually all biological phenomena—from individual physiology to interspecific relationships to global nutrient fluxes—have annual cycles and are influenced by the timing of abiotic events. Recent years have seen a surge of interest in this topic, as an increasing number of studies document phenological responses to climate change. Much recent research has addressed the genetic controls on phenology, modelling techniques and ecosystem-level and evolutionary consequences of phenological change. To date, however, these efforts have tended to proceed independently. Here, we bring together some of these disparate lines of inquiry to clarify vocabulary, facilitate comparisons among habitat types and promote the integration of ideas and methodologies across different disciplines and scales. We discuss the relationship between phenology and life history, the distinction between organismal- and population-level perspectives on phenology and the influence of phenology on evolutionary processes, communities and ecosystems. Future work should focus on linking ecological and physiological aspects of phenology, understanding the demographic effects of phenological change and explicitly accounting for seasonality and phenology in forecasts of ecological and evolutionary responses to climate change.     

Experimental analysis of an early life‐history stage: avian predation selects for larger body size of hatchling turtles

One common life‐history pattern involves an elevated rate and nonrandom distribution of neonatal mortality. However, the mechanisms causing this pattern and the specific traits that confer a survival benefit are not always evident. We conducted a manipulative field experiment using red‐eared slider turtles to test the hypothesis that diurnal avian predators are a primary cause of size‐specific neonatal mortality. Body size was a significant predictor of recapturing hatchlings alive and of finding hatchlings dead under natural conditions, but was unimportant when diurnal predators were excluded from the field site. Overall recapture rates also more than doubled when predators were excluded compared to natural conditions (72.4 vs. 34.9%). We conclude that birds are an important cause of size‐specific mortality of recently emerged hatchling turtles and that ‘bigger is better’ in this system, which has important implications for life‐history evolution in organisms that experience size‐specific neonatal mortality.     

Correlated evolution of sex and reproductive mode in corals (Anthozoa: Scleractinia)

Sexuality and reproductive mode are two fundamental life-history traits that exhibit largely unexplained macroevolutionary patterns among the major groups of multicellular organisms. For example, the cnidarian class Anthozoa (corals and anemones) is mainly comprised of gonochoric (separate sex) brooders or spawners, while one order, Scleractinia (skeleton-forming corals), appears to be mostly hermaphroditic spawners. Here, using the most complete phylogeny of scleractinians, we reconstruct how evolutionary transitions between sexual systems (gonochorism versus hermaphrodism) and reproductive modes (brooding versus spawning) have generated large-scale taxonomic patterns in these characters. Hermaphrodites have independently evolved in three large, distantly related lineages consisting of mostly reef-building species. Reproductive mode in corals has evolved at twice the rate of sexuality, while the evolution of sexuality has been heavily biased: gonochorism is over 100 times more likely to be lost than gained, and can only be acquired by brooders. This circuitous evolutionary pathway accounts for the prevalence of hermaphroditic spawners among reef-forming scleractinians, despite their ancient gonochoric heritage.     

Life history evolution in cichlids 2: directional evolution of the trade-off between egg number and egg size

The negative relationship between offspring number and offspring size provides a classic example of the role of trade-offs in life history theory. However, the evolutionary transitions in egg size and clutch size that have produced this negative relationship are still largely unknown. Since body size may affect both of these traits, it would be helpful to understand how evolutionary changes in body size may have facilitated or constrained shifts in clutch and egg size. By using comparative methods with a database of life histories and a phylogeny of 222 genera of cichlid fishes, we investigated the order of evolutionary transitions in these traits in relation to each other. We found that the ancestral large-bodied cichlids first increased egg size, followed by a decrease in both body size and clutch size resulting in the common current combination of a small-bodied cichlid with a small clutch of large eggs. Furthermore, lineages that deviated from the negative relationship between clutch and egg size underwent different transitions in these traits according to their body size (large bodied genera have moved towards the large clutch/small egg end of the continuum and small bodied genera towards the small clutch/large egg end of the continuum) to reach the negative relationship between clutch size and egg size. Our results show that body size is highly important in shaping the negative relationship between clutch size and egg size.     

The evolution of parental care in shorebirds: life histories, ecology, and sexual selection

Parental care is expected to evolve according to a trade-offbetween the benefits of increased survival of offspring andcosts of reduced survival and future reproduction of adults.Here we investigate the components of this life-history trade-offin shorebirds (Charadriides, excluding Laroidea), an avian infraorderdisplaying an unusual diversity in extent of care by each sex.We show that evolutionary increases in the duration of carein one sex are associated with decreased care by the other.We found no evidence that various hypothesised benefits of careprovide a general explanation for the duration of care by eitheror both sexes, although parental feeding of the young was tooconservative for comparisons. Sexual dimorphism in body sizehad a similar relationship to parental care in both sexes: reductionsin duration of care by either sex were matched by increasesin the size of that sex relative to the other. Whereas thispattern could be explained by sexual selection in males, itwas retained within socially monogamous females. Reduced carein males (but not in females) appears to have facilitated theevolution of greater migration distances. These results suggestthat parental care has had different causes and consequencesin each sex. Benefits of desertion due to sexual selection aremore clearly demonstrable for males, whereas correlates of careare less clear for females     

Covariation between brain size and immunity in birds: implications for brain size evolution

Parasitism can negatively affect learning and cognition, setting the scene for coevolution between brain and immunity. Greater susceptibility to parasitism by males may impair their cognitive ability, and relatively greater male investment in immunity could compensate for greater susceptibility to parasites, in particular when males have a relatively large brain. We analysed covariation between relative size of immune defence organs and brain in juvenile and adult birds. The relative size of the bursa of Fabricius and the spleen in adults covaried positively with relative brain size across bird species. The relative size of these two immune defence organs covaried with sex differences in relative size of the brain, indicating that the relationship between immune defence and brain size was stronger for males. In contrast, liver and heart size or sexual size dimorphism in size did not covary with immune defence. Thus, species in which males have relatively large brains also have relatively large immune defence organs.     

Maternal effects and heritability of annual productivity

Within-individual consistency and among-individual heterogeneity in fitness are prerequisites for selection to take place. Within-individual variation in productivity between years, however, can vary considerably, especially when organisms become older and more experienced. We examine individual consistency in annual productivity, the covariation between survival and annual productivity, and the sources of variation in annual productivity, while accounting for advancing age, to test the individual-quality and resource-allocation life-history theory hypotheses. We use long-term data from a pedigreed, wild population of house sparrows. Within-individual annual productivity first increased and later decreased with age, but there were no selective mortality due to individual quality and no correlation between lifespan and productivity. Individuals were consistent in their annual productivity (C = 0.49). Narrow-sense heritability was low (h(2) = 0.09), but maternal effects explained much of the variation (M = 0.33). Such effects can influence evolutionary processes and are of major importance for our understanding of how variation in fitness can be maintained.     

A mitogenomic timescale for birds detects variable phylogenetic rates of molecular evolution and refutes the standard molecular clock

Current understanding of the diversification of birds is hindered by their incomplete fossil record and uncertainty in phylogenetic relationships and phylogenetic rates of molecular evolution. Here we performed the first comprehensive analysis of mitogenomic data of 48 vertebrates, including 35 birds, to derive a Bayesian timescale for avian evolution and to estimate rates of DNA evolution. Our approach used multiple fossil time constraints scattered throughout the phylogenetic tree and accounts for uncertainties in time constraints, branch lengths, and heterogeneity of rates of DNA evolution. We estimated that the major vertebrate lineages originated in the Permian; the 95% credible intervals of our estimated ages of the origin of archosaurs (258 MYA), the amniote-amphibian split (356 MYA), and the archosaur-lizard divergence (278 MYA) bracket estimates from the fossil record. The origin of modern orders of birds was estimated to have occurred throughout the Cretaceous beginning about 139 MYA, arguing against a cataclysmic extinction of lineages at the Cretaceous/Tertiary boundary. We identified fossils that are useful as time constraints within vertebrates. Our timescale reveals that rates of molecular evolution vary across genes and among taxa through time, thereby refuting the widely used mitogenomic or cytochrome b molecular clock in birds. Moreover, the 5-Myr divergence time assumed between 2 genera of geese (Branta and Anser) to originally calibrate the standard mitochondrial clock rate of 0.01 substitutions per site per lineage per Myr (s/s/l/Myr) in birds was shown to be underestimated by about 9.5 Myr. Phylogenetic rates in birds vary between 0.0009 and 0.012 s/s/l/Myr, indicating that many phylogenetic splits among avian taxa also have been underestimated and need to be revised. We found no support for the hypothesis that the molecular clock in birds "ticks" according to a constant rate of substitution per unit of mass-specific metabolic energy rather than per unit of time, as recently suggested. Our analysis advances knowledge of rates of DNA evolution across birds and other vertebrates and will, therefore, aid comparative biology studies that seek to infer the origin and timing of major adaptive shifts in vertebrates.     

Modelling contemporary evolution in stickleback

During the past decade, two lines of research have advanced our understanding of micro‐evolution. On the one hand, a number of studies have generated evidence for strong selection on phenotypes ( Kingsolver et al. 2001 ) and the contemporary (sometimes deemed ‘rapid’) evolution of phenotypic traits ( Hendry & Kinnison 1999 ). On the other hand, other studies have sought to identify the genes that underlie ecologically important traits ( Ungerer et al. 2008 ). Over the next decade, micro‐evolutionists might expect considerable progress from the study of contemporary evolution at both the phenotypic and genetic level simultaneously. In this issue of Molecular Ecology, Le Rouzic et al. (2011) present a teaser for this approach. They examined contemporary evolution of an adaptive trait with a well‐studied genetic basis, the number of lateral plates, in threespine stickleback (Gasterosteus aculeatus L.). A time series of 20 years of change for this trait after introduction into a pond in Norway was compared with a similar time series of 12 years following the invasion of a lake in Alaska. Using a modelling approach, the authors then teased apart selection acting upon the phenotype and selection acting on a major effect gene. In both time series, selection was strong and consistent. The models suggested that selection could act directly on the phenotype, or through the gene’s pleiotropic effects.     

Correlated evolution of colour pattern and body size in polymorphic pygmy grasshoppers, Tetrix undulata

Theory posits that selection on functionally interrelated characters will promote physical and genetic integration resulting in evolution of favourable trait-value combinations. The pygmy grasshopper Tetrix undulata (Orthoptera: Tetrigidae) displays a genetically encoded polymorphism for colour pattern. Colour morphs differ in several traits, including behaviours, thermal biology and body size. To examine if these size differences may reflect phenotypic plasticity of growth and development in response to temperature we used a split brood-design and reared hatchlings from mothers belonging to different morphs in different thermal environments (warm or cold) until maturity. We found that time to maturity was longer in the cold compared with the warm treatment. In the warm (but not in the cold) treatment time to maturity also varied among individuals born to mothers belonging to different colour morphs. Although low temperature and long development time are normally accompanied by increased body size in ectotherms, our results revealed no difference in size at maturity between individuals reared in the two temperature treatments. There was also an increase (not a decrease) in adult body size with shortened time to maturity across families within each treatment. Taken together, this suggests that body size is canalized against environmental perturbations, and that early maturation does not necessarily trade off against a size-mediated decrease in fecundity. Heritability of body size was moderate in magnitude. Moreover, body size at maturity varied among individuals belonging to different morphs and was influenced also by maternal colour morph, suggesting that a genetic correlation exists between colour pattern and body size. These findings suggest that different characters have evolved in concert and that the various colour morphs represent different evolutionary strategies, i.e., alternative peaks in a multi-modal adaptive landscape.     

The fossil record and limb disparity of enantiornithines, the dominant flying birds of the Cretaceous

Morphometric and stratigraphic analyses that encompass the known fossil record of enantiornithine birds (Enantiornithes) are presented. These predominantly flighted taxa were the dominant birds of the second half of the Mesozoic; the enantiornithine lineage is known to have lasted for at least 60 million years (Ma), up until the end of the Cretaceous. Analyses of fossil record dynamics show that enantiornithine 'collectorship' since the 1980s approaches an exponential distribution, indicating that an asymptote in proportion of specimens has yet to be achieved. Data demonstrate that the fossil record of enantiornithines is complete enough for the extraction of biological patterns. Comparison of the available fossil specimens with a large data set of modern bird (Neornithes) limb proportions also illustrates that the known forelimb proportions of enantiornithines fall within the range of extant taxa; thus these birds likely encompassed the range of flight styles of extant birds. In contrast, most enantiornithines had hindlimb proportions that differ from any extant taxa. To explore this, ternary diagrams are used to graph enantiornithine limb variation and to identify some morphological oddities ( Otogornis , Gobipteryx ); taxa not directly comparable to modern birds. These exceptions are interesting – although anatomically uniform, and similar to extant avians in their wing proportions, some fossil enantiornithines likely had flight styles not seen among their living counterparts.     

The origin and early evolution of birds

Birds evolved from and are phylogenetically recognized as members of the theropod dinosaurs; their first known member is the Late Jurassic Archaeopteryx, now represented by seven skeletons and a feather, and their closest known non-avian relatives are the dromaeosaurid theropods such as Deinonychus. Bird flight is widely thought to have evolved from the trees down, but Archaeopteryx and its outgroups show no obvious arboreal or tree-climbing characters, and its wing planform and wing loading do not resemble those of gliders. The ancestors of birds were bipedal, terrestrial, agile, cursorial and carnivorous or omnivorous. Apart from a perching foot and some skeletal fusions, a great many characters that are usually considered ‘avian’ (e.g. the furcula, the elongated forearm, the laterally flexing wrist and apparently feathers) evolved in non-avian theropods for reasons unrelated to birds or to flight. Soon after Archaeopteryx, avian features such as the pygostyle, fusion of the carpometacarpus, and elongated curved pedal claws with a reversed, fully descended and opposable hallux, indicate improved flying ability and arboreal habits. In the further evolution of birds, characters related to the flight apparatus phylogenetically preceded those related to the rest of the skeleton and skull. Mesozoic birds are more diverse and numerous than thought previously and the most diverse known group of Cretaceous birds, the Enantiornithes, was not even recognized until 1981. The vast majority of Mesozoic bird groups have no Tertiary records: Enantiornithes, Hesperornithiformes, Ichthyornithiformes and several other lineages disappeared by the end of the Cretaceous. By that time, a few Linnean ‘Orders’ of extant birds had appeared, but none of these taxa belongs to extant ‘families’, and it is not until the Paleocene or (in most cases) the Eocene that the majority of extant bird ‘Orders’ are known in the fossil record. There is no evidence for a major or mass extinction of birds at the end of the Cretaceous, nor for a sudden ‘bottleneck’ in diversity that fostered the early Tertiary origination of living bird ‘Orders’.     

The evolution of reaction norms: simple models for age and size at maturity

This paper presents a simple model for the evolution of reaction norms for age and size at maturity that predicts reaction norms with a variety of shapes. Using realistic parameter values the model predicts reaction norms close to those observed in Drosophila. The major assumptions of the model are: 1) that net reproductive rate is maximized, 2) that growth is determinate, and 3) that mortality rates are independent of age and size at maturity. If, additionally, juvenile mortality is uncorrelated with a growth coefficient, k, the model predicts that selection favors maturation later at a smaller size when k is reduced by environmental factors and that decreased juvenile mortality leads to delayed maturity. These two predictions conform with those found by previous models using other measures of fitness. Correlations between k and juvenile mortality can change the shape of the predicted reaction norm. Depending on the precise form of the correlation, the model can predict done- or bowl-shaped reaction norms and can predict delayed or earlier maturity as k decreases. These shapes are qualitatively different from those predicted by previous models that used different fitness measures. Systematic estimates of the parameter values for this and for related models are required to determine the appropriate fitness measure for models of reaction norms.