Co-evolutionary dynamics of mammalian brain and body size.

Despite decades of comparative studies, puzzling aspects of the relationship between mammalian brain and body mass continue to defy satisfactory explanation. Here we show that several such aspects arise from routinely fitting log-linear models to the data: the correlated evolution of brain and body mass is in fact log-curvilinear. This simultaneously accounts for several phenomena for which diverse biological explanations have been proposed, notably variability in scaling coefficients across clades, low encephalization in larger species and the so-called taxon-level problem. Our model implies a need to revisit previous findings about relative brain mass. Accounting for the true scaling relationship, we document dramatically varying rates of relative brain mass evolution across the mammalian phylogeny, and we resolve the question of whether there is an overall trend for brain mass to increase through time. We find a trend in only three mammalian orders, which is by far the strongest in primates, setting the stage for the uniquely rapid directional increase ultimately producing the computational powers of the human brain.

Taste shaped the use of botanical drugs.

The perception of taste and flavour (a combination of taste, smell, and chemesthesis), here also referred to as chemosensation, enables animals to find high-value foods and avoid toxins. Humans have learned to use unpalatable and toxic substances as medicines, yet the importance of chemosensation in this process is poorly understood. Here, we generate tasting-panel data for botanical drugs and apply phylogenetic generalised linear mixed models to test whether intensity and complexity of chemosensory qualities as well as particular tastes and flavours can predict ancient Graeco-Roman drug use. We found chemosensation to be strongly predictive of therapeutic use: botanical drugs with high therapeutic versatility have simple yet intense tastes and flavours, and 21 of 22 chemosensory qualities predicted at least one therapeutic use. In addition to the common notion of bitter tasting medicines, we also found starchy, musky, sweet, and soapy drugs associated with versatility. In ancient Greece and Rome, illness was thought to arise from imbalance in bodily fluids or humours, yet our study suggests that uses of drugs were based on observed physiological effects that are often consistent with modern understanding of chemesthesis and taste receptor pharmacology.

In ancient times people used trial and error to identify medicinal plants as being effective. Later, diseases were believed to arise from imbalances in body fluids (or 'humours'), and botanical drugs were thought to restore this balance through the power of their taste. Modern science rejects this theory but does recognise the importance of chemosensation ­ our sensitivity to chemicals through taste and smell. These senses evolved in humans to help us seek out nutrients and avoid toxins and may also have guided the ancient uses of botanical drugs. There are many records of historical medicinal plant use and ailments, which makes it possible to explore possible relationships between therapeutic uses of botanical drugs and their chemosensory qualities. To investigate if therapeutic uses of botanical drugs could indeed be predicted by taste and flavour, Leonti, Baker et al. collected 700 botanical drugs identified in an ancient text, named De Materia Medica, which dates back to the 1^st century CE. The researchers asked volunteer tasters to classify the botanical drugs using 22 taste descriptions, such as bitter, aromatic, burning/hot, and fresh/cooling. The volunteers were also asked to score the strength of these tastes. Leonti, Baker et al. then used statistical modelling to see if the participant's taste descriptions could be used to predict the therapeutic uses of the drugs identified in the ancient text. This revealed that of the 46 therapeutic indications described in the text, 45 showed significant associations with at least one taste quality. Botanical drugs with stronger and simpler tastes tended to be used for a wider range of therapeutic indications. This suggests that chemosensation influenced therapeutic expectations in ancient, prescientific medicine. The study of Leonti, Baker et al. brings ancient medicine to life, offering valuable insights into the chemosensory aspects of medicinal plants and their potential applications in modern medicine. A next step would be to explore whether these insights could have relevance to modern science.

Genes underlying the evolution of tetrapod testes size.

BACKGROUND: Testes vary widely in mass relative to body mass across species, but we know very little about which genes underlie and contribute to such variation. This is partly because evidence for which genes are implicated in testis size variation tends to come from investigations involving just one or a few species. Contemporary comparative phylogenetic methods provide an opportunity to test candidate genes for their role in phenotypic change at a macro-evolutionary scale-across species and over millions of years. Previous attempts to detect genotype-phenotype associations across species have been limited in that they can only detect where genes have driven directional selection (e.g. brain size increase). RESULTS: Here, we introduce an approach that uses rates of evolutionary change to overcome this limitation to test whether any of twelve candidate genes have driven testis size evolution across tetrapod vertebrates-regardless of directionality. We do this by seeking a relationship between the rates of genetic and phenotypic evolution. Our results reveal five genes (Alkbh5, Dmrtb1, Pld6, Nlrp3, Sp4) that each have played unique and complex roles in tetrapod testis size diversity. In all five genes, we find strong significant associations between the rate of protein-coding substitutions and the rate of testis size evolution. Such an association has never, to our knowledge, been tested before for any gene or phenotype. CONCLUSIONS: We describe a new approach to tackle one of the most fundamental questions in biology: how do individual genes give rise to biological diversity? The ability to detect genotype-phenotype associations that have acted across species has the potential to build a picture of how natural selection has sculpted phenotypic change over millions of years.

Nothing Wrong with the Analysis of Clades in Comparative Evolutionary Studies: A Reply to Poe et al.

In a recent paper, Poe et al. assert that scientists should abandon clade-based approaches, particularly those using named taxonomic ranks. Poe et al. attempt to demonstrate that clade selection can have effects on the results of evolutionary analyses but unfortunately fall short of making any robust conclusions. Here, we demonstrate that the assertions made by Poe et al. have two important flaws: (i) an erroneous view of modern phylogenetic comparative methods; and (ii) a lack of statistical rigor in their analyses. We repeat Poe et al.'s analysis but using appropriate phylogenetic comparative approaches. We demonstrate that results remain consistent regardless of the clade definition. We go on to discuss the value of taxonomic groupings and how they can provide meaningful units of comparison in evolutionary study. Unlike the disheartening suggestion to abandon the use of clades, scientists can instead continue to use phylogenetic " corrections" that are already the standard for most comparative evolutionary analyses. [Comparative methods; evolution; phylogeny; taxonomy.].

150 million years of sustained increase in pterosaur flight efficiency.

The long-term accumulation of biodiversity has been punctuated by remarkable evolutionary transitions that allowed organisms to exploit new ecological opportunities. Mesozoic flying reptiles (the pterosaurs), which dominated the skies for more than 150 million years, were the product of one such transition. The ancestors of pterosaurs were small and probably bipedal early archosaurs1, which were certainly well-adapted to terrestrial locomotion. Pterosaurs diverged from dinosaur ancestors in the Early Triassic epoch (around 245 million years ago); however, the first fossils of pterosaurs are dated to 25 million years later, in the Late Triassic epoch. Therefore, in the absence of proto-pterosaur fossils, it is difficult to study how flight first evolved in this group. Here we describe the evolutionary dynamics of the adaptation of pterosaurs to a new method of locomotion. The earliest known pterosaurs took flight and subsequently appear to have become capable and efficient flyers. However, it seems clear that transitioning between forms of locomotion2,3-from terrestrial to volant-challenged early pterosaurs by imposing a high energetic burden, thus requiring flight to provide some offsetting fitness benefits. Using phylogenetic statistical methods and biophysical models combined with information from the fossil record, we detect an evolutionary signal of natural selection that acted to increase flight efficiency over millions of years. Our results show that there was still considerable room for improvement in terms of efficiency after the appearance of flight. However, in the Azhdarchoidea4, a clade that exhibits gigantism, we test the hypothesis that there was a decreased reliance on flight5-7 and find evidence for reduced selection on flight efficiency in this clade. Our approach offers a blueprint to objectively study functional and energetic changes through geological time at a more nuanced level than has previously been possible.

Female-driven intersexual coevolution in beetle genitalia.

Genital coevolution is a pervasive phenomenon as changes in one sex tend to impose fitness consequences on the other, generating sexual conflict. Sexual conflict is often thought to cause stronger selection on males due to the Darwin-Bateman's anisogamy paradigm. However, recent studies have demonstrated that female genitalia may be equally elaborated and perform diverse extra-copulatory functions. These characteristics suggest that female genitals can also be primary targets of selection, especially where natural selection acts on female-exclusive functions such as oviposition. Here, we test this hypothesis in a statistical phylogenetic framework across the whole beetle (Coleoptera) phylogeny, investigating whether coevolution of specific genital traits may be triggered by changes in females. We focus on traits of the proctiger, which composes part of the male terminalia and the female ovipositor. Our results present a comprehensive case of male-female genital coevolution and provide solid statistical evidence for a female-initiated coevolutionary process where the vast majority of evolutionary transitions in males have occurred only after changes in females. We corroborate the hypothesis that female traits may change independently and elicit counter-adaptations in males. Furthermore, by showing a consistent pattern across the phylogeny of the most diverse group of animals, our results suggest that this female-driven dynamics may persist through long time scales.

Rapid decreases in relative testes mass among monogamous birds but not in other vertebrates.

Larger testes produce more sperm and therefore improve reproductive success in the face of sperm competition. Adaptation to social mating systems with relatively high and low sperm competition are therefore likely to have driven changes in relative testes size in opposing directions. Here, we combine the largest vertebrate testes mass dataset ever collected with phylogenetic approaches for measuring rates of morphological evolution to provide the first quantitative evidence for how relative testes mass has changed over time. We detect explosive radiations of testes mass diversity distributed throughout the vertebrate tree of life: bursts of rapid change have been frequent during vertebrate evolutionary history. In socially monogamous birds, there have been repeated rapid reductions in relative testes mass. We see no such pattern in other monogamous vertebrates; the prevalence of monogamy in birds may have increased opportunities for investment in alternative behaviours and physiologies allowing reduced investment in expensive testes.

Rapid Change in Mammalian Eye Shape Is Explained by Activity Pattern.

The rate of morphological evolution along the branches of a phylogeny varies widely [1-6]. Although such rate variation is often assumed to reflect the strength of historical natural selection resulting in adaptation [7-14], this lacks empirical and analytical evidence. One way to demonstrate a relationship between branchwise rates and adaptation would be to show that rapid rates of evolution are linked with ecological shifts or key innovations. Here, we test for this link by determining whether activity pattern, the time of day at which species are active, explains rapid bursts of evolutionary change in eye shape. Using modern approaches to identify shifts in the rate of morphological evolution [7, 13], we find that over 74% of rapid eye-shape change during mammalian evolutionary history is directly explained by distinct selection pressures acting on nocturnal, cathemeral, and diurnal species. Our results reveal how ecological changes occurring along the branches of a phylogeny can manifest in subsequent changes in the rate of morphological evolution. Although selective pressures exerted by different activity patterns have acted uniformly across all mammals, we find differences in the rate of eye-shape evolution among orders. The key to understanding this is in how ecology itself has evolved. We find heterogeneity in how activity pattern has evolved among mammals that ultimately led to differences in the rate of eye-shape evolution among species. Our approach represents an exciting new way to pinpoint factors driving adaptation, enabling a clearer understanding of the factors that drive the evolution of biological diversity.

Fundamental insights into ontogenetic growth from theory and fish.

The fundamental features of growth may be universal, because growth trajectories of most animals are very similar, but a unified mechanistic theory of growth remains elusive. Still needed is a synthetic explanation for how and why growth rates vary as body size changes, both within individuals over their ontogeny and between populations and species over their evolution. Here, we use Bertalanffy growth equations to characterize growth of ray-finned fishes in terms of two parameters, the growth rate coefficient, K, and final body mass, m∞. We derive two alternative empirically testable hypotheses and test them by analyzing data from FishBase. Across 576 species, which vary in size at maturity by almost nine orders of magnitude, K scaled as [Formula: see text]. This supports our first hypothesis that growth rate scales as [Formula: see text] as predicted by metabolic scaling theory; it implies that species that grow to larger mature sizes grow faster as juveniles. Within fish species, however, K scaled as [Formula: see text]. This supports our second hypothesis, which predicts that growth rate scales as [Formula: see text] when all juveniles grow at the same rate. The unexpected disparity between across- and within-species scaling challenges existing theoretical interpretations. We suggest that the similar ontogenetic programs of closely related populations constrain growth to [Formula: see text] scaling, but as species diverge over evolutionary time they evolve the near-optimal [Formula: see text] scaling predicted by metabolic scaling theory. Our findings have important practical implications because fish supply essential protein in human diets, and sustainable yields from wild harvests and aquaculture depend on growth rates.

The role of life history traits in mammalian invasion success.

Why some organisms become invasive when introduced into novel regions while others fail to even establish is a fundamental question in ecology. Barriers to success are expected to filter species at each stage along the invasion pathway. No study to date, however, has investigated how species traits associate with success from introduction to spread at a large spatial scale in any group. Using the largest data set of mammalian introductions at the global scale and recently developed phylogenetic comparative methods, we show that human-mediated introductions considerably bias which species have the opportunity to become invasive, as highly productive mammals with longer reproductive lifespans are far more likely to be introduced. Subsequently, greater reproductive output and higher introduction effort are associated with success at both the establishment and spread stages. High productivity thus supports population growth and invasion success, with barriers at each invasion stage filtering species with progressively greater fecundity.

Adaptive evolution toward larger size in mammals.

The notion that large body size confers some intrinsic advantage to biological species has been debated for centuries. Using a phylogenetic statistical approach that allows the rate of body size evolution to vary across a phylogeny, we find a long-term directional bias toward increasing size in the mammals. This pattern holds separately in 10 of 11 orders for which sufficient data are available and arises from a tendency for accelerated rates of evolution to produce increases, but not decreases, in size. On a branch-by-branch basis, increases in body size have been more than twice as likely as decreases, yielding what amounts to millions and millions of years of rapid and repeated increases in size away from the small ancestral mammal. These results are the first evidence, to our knowledge, from extant species that are compatible with Cope's rule: the pattern of body size increase through time observed in the mammalian fossil record. We show that this pattern is unlikely to be explained by several nonadaptive mechanisms for increasing size and most likely represents repeated responses to new selective circumstances. By demonstrating that it is possible to uncover ancient evolutionary trends from a combination of a phylogeny and appropriate statistical models, we illustrate how data from extant species can complement paleontological accounts of evolutionary history, opening up new avenues of investigation for both.