Ontogeny and phylogeny of mating behaviour: social heteroch rony in primates.

Based on the Recognition Concept of species, the specific-mate contact model posits that mating systems develop as combinations of two fundamental courtship strategies that we interpret here in terms of behavioural heterochrony: territorial mate-attraction evolved as an effect of peramorphosis whereas group-living mate-seeking evolved as an effect of paedomorphosis. We tested this hypothesis on primates in a phylogenetic and paleo-climatic context. Our results suggest that primate promiscuity (both males and females are mate-seekers) evolved with group-living from ancestral pair-living monogamy (both males and females are mate-attractors) in the Palaeogene, as the result of a slowdown in growth (neoteny) caused by increased environmental predictability. A secondary return to territorial monogamy probably evolved as the result of accelerated growth driven by seasonality (acceleration). Polygamy evolved in the Neogene during periods of forest fragmentation and environmental unpredictability. Small monogamous ancestors evolved seasonal polyandry (female attraction) as an effect of truncated development (progenesis). Large promiscuous, neotenic ancestors evolved non-seasonal polygyny (male attraction) as an effect of prolonged development (hypermorphosis) in males. We conclude that social heterochrony offers alternative explanations for the coevolution of life history and mating be-haviour; and we discuss the implications of our model for human social evolution.

Pith width, leaf size, and twig thickness.

PREMISE: To support large leaves, many woody plant species evolved a cost-effective way to thicken twigs. As an extension of E. J. H. Corner's rule that twig diameter increases with leaf size, we hypothesized that pith width also increases with leaf size. The benefit to the plant from the proposed relationship is that pith is a low-cost tissue that reduces the metabolic cost of large diameter twig production. METHODS: Leaf sizes and cross-sectional areas of bark, xylem, and pith of 81 species of trees and shrubs growing in Gainesville, Florida were measured and compared with standardized major axis regressions of pairwise species trait values and phylogenetically independent contrasts. RESULTS: Pith area increases with leaf size with or without accounting for phylogenetic relationships. In agreement with Corner's rule, overall twig diameter as well as bark and wood thickness also increase with leaf size. Thicker twigs showed more variation in relative pith, wood, and bark cross-sectional areas compared to thinner twigs. CONCLUSIONS: Investments in pith, a tissue of low density found in the centers of twigs, provides a low-cost way to increase twig circumference and thereby space for attachment of large leaves while increasing the overall second moment of area of twigs, which increases their ability to biomechanically support large leaves.

Using BayesModelS to provide Bayesian- and phylogenetically-informed primate body mass predictions.

An accurate prediction of the body mass of an extinct species can greatly inform the reconstruction of that species' ecology. Therefore, paleontologists frequently predict the body mass of extinct taxa from fossilized materials, particularly dental dimensions. Body mass prediction has traditionally been performed in a frequentist statistical framework, and accounting for phylogenetic relationships while calibrating prediction models has only recently become more commonplace. In this article, we apply BayesModelS-a phylogenetically informed Bayesian prediction method-to predict body mass in a sample of 49 euarchontan species (24 strepsirrhines, 20 platyrrhines, 3 tarsiids, 1 dermopteran, and 1 scandentian) and compare this approach's body mass prediction accuracy with other commonly used techniques, namely ordinary least squares, phylogenetic generalized least squares, and phylogenetic independent contrasts (PICs). When predicting the body masses of extant euarchontans from dental and postcranial variables, BayesModelS and PICs have substantially higher predictive accuracy than ordinary least squares and phylogenetic generalized least squares. The improved performances of BayesModelS and PIC are most evident for dentally derived body mass proxies or when body mass proxies have high degrees of phylogenetic covariance. Predicted values generated by BayesModelS and PIC methods also show less variance across body mass proxies when applied to the Eocene adapiform Notharctus tenebrosus. These more explicitly phylogenetically based methods should prove useful for predicting body mass in a paleontological context, and we provide executive scripts for both BayesModelS and PIC to increase ease of application.

Interspecific variation in mortality and growth and changes in their relationship with size class in an old-growth temperate forest.

Understanding trade-offs between demographic parameters is crucial when investigating community assembly rules in high-diversity forests. To this end, we estimated mortality and growth parameters, and correlations among them, across entire size classes for 17 tree species (Betula, Carpinus, Fagus, Quercus, Castanea, Acer, Cerasus, Swida, Kalopanax, and Styrax) using a dataset over 18 years obtained from an old-growth forest in Japan.Size classes were represented by 12 categories determined by age, height, and diameter at breast height (DBH) from new seedlings to stems of DBH >85 cm. We derived the annual mortality and growth for each species and class using estimates of transition probabilities between classes. Trade-offs or synergies in growth and survival among species per size class were analyzed with and without the inclusion of phylogenetic relationships.Annual mortality showed U-shaped patterns across size classes for species that could potentially reach a DBH ≥55 cm: 0.2-0.98 for seedlings, 0.002-0.01 at DBH 35-45 cm, and ca. 0.01 at DBH ≥55 cm. Other species demonstrated monotonically decreasing mortality toward specific maximum size classes. When phylogenetic information was included in analyses, the correlations between survival and growth changed across size classes were significant for some classes: As an overall tendency, synergy was observed in growth and survival for seedling to sapling classes, trade-offs for juvenile to DBH 15-25 cm classes, and synergy again for larger classes. When phylogenetic information was not included, a significant trade-off was observed only at DBH 5-15 cm. Synthesis. Trade-offs at intermediate classes imply differentiation in demographic characteristics related to life history strategies. However, evolutionarily obtained demographic characteristics are not substantial drivers of niche differentiation in the study area. The polylemma of mortality, growth, and other parameters such as the onset of reproduction may also be important factors driving species-specific demographic traits.

The reproductive period of tarantulas is constrained by their thermal preferences (Araneae, Theraphosidae).

Locomotor and physiological performance of ectotherms are affected by temperature. Thermoregulation is achieved by changes in behavior and the selection of micro-habitats with adequate temperatures to maintain the body temperature (Tb) within a range of preference. Apart from this temperature dependence at spatial scales, ectotherms are also affected by temperature at temporal scale. For instance, ectotherms can only be active some months of the year, particularly in temperate environments. Tarantulas are ectotherms that live in burrows most of their life. Nevertheless, after the sexual maturation molt, males leave their refugia and start a wandering life searching for females to mate. The reproductive period varies among species. In some species walking males are seen in late spring or early summer, while in other species males are only seen during fall or winter. Apart from the differences in lifestyles after maturation, tarantulas exhibit sexual dimorphisms in longevity and body mass, having smaller, shorter-lived males. Thus, to optimize energetic budgets, decreasing thermoregulation costs, we hypothesize and examine a putative correlation between an individual's preferred body temperature (Tpref) and the environmental temperature during the reproductive period. Hence, we characterize Tpref in seven tarantula species and analyze which factors (i.e., time of day, body mass, and sex) correlated with it. Furthermore, we assess putative correlated evolution of Tpref with ambient temperature (minima, mean, and maxima) during the reproductive period by means of phylogenetic independent contrasts. We did not find differences in thermal preferences between sexes; and only one species, Acanthoscurria suina, exhibited diel differences in Tpref. We found evidence of correlated evolution between Tpref and minimum temperature during the reproductive period among all seven species studied herein. Our results show that the reproductive period is constrained by thermal preferences, dictating when males can start their wandering life to mate.

Interspecific variation in hypoxia tolerance and hypoxia acclimation responses in killifish from the family Fundulidae.

Hypoxia is a pervasive stressor in aquatic environments, and both phenotypic plasticity and evolutionary adaptation could shape the ability to cope with hypoxia. We investigated evolved variation in hypoxia tolerance and the hypoxia acclimation response across fundulid killifishes that naturally experience different patterns of hypoxia exposure. We compared resting O2 consumption rate (MO2 ), and various indices of hypoxia tolerance [critical O2 tension (Pcrit), regulation index (RI), O2 tension (PO2 ) at loss of equilibrium (PLOE) and time to LOE (tLOE) at 0.6 kPa O2] in Fundulus confluentus, Fundulus diaphanus, Fundulus heteroclitus, Fundulus rathbuni, Lucania goodei and Lucania parva We examined the effects of chronic (28 days) exposure to constant hypoxia (2 kPa) or nocturnal intermittent hypoxia (12 h normoxia:12 h hypoxia) in a subset of species. Some species exhibited a two-breakpoint model in MO2  caused by early, modest declines in MO2  in moderate hypoxia. We found that hypoxia tolerance varied appreciably across species: F. confluentus was the most tolerant (lowest PLOE and Pcrit, longest tLOE), whereas F. rathbuni and F. diaphanus were the least tolerant. However, there was not a consistent pattern of interspecific variation for different indices of hypoxia tolerance, with or without taking phylogenetic relatedness into account, probably because these different indices are underlain by partially distinct mechanisms. Hypoxia acclimation generally improved hypoxia tolerance, but the magnitude of plasticity and responsiveness to different hypoxia patterns varied interspecifically. Our results therefore suggest that hypoxia tolerance is a complex trait that is best appreciated by considering multiple indices of tolerance.

Dispersal mode constrains allocation of carbon and mineral nutrients in seeds of forest and savanna trees.

Species vary in seed size and content of stored reserves, which can be related to dispersal strategies and type of habitat in which they are found. We compare seed carbon and nutrient reserves of anemochorous and zoochorous trees from the Cerrado of central Brazil. We measured seed dry mass, lipids, non-structural carbohydrates (starch and total soluble sugars), carbon and mineral nutrients in ten forest and 13 savanna species, each classified as having wind- or animal-dispersed seeds. We used phylogenetically independent contrasts to test for correlations among these traits. Seeds of anemochorous species were lighter, with higher concentrations of C, N, P, Ca and Mg. Lipids were the dominant carbon reserve for most anemochorous species, underpinning the importance of allocation to compact carbon reserves. Starch, lipids or soluble sugars were the major carbon reserve in zoochorous seeds. Savanna and forest species did not differ in seed mass or in total carbon reserves. However, seeds of forest species had higher concentrations of starch than seeds of savanna species. Lipid and starch negatively correlated across species, suggesting a trade-off between starch and lipids as major seed carbon reserves. Calcium was positively correlated with Mn and B, while Mg was positively correlated with C, N, P, K, S, Zn and B. Potassium, S and Cl were positively correlated, while P was positively correlated with Mg and Zn. Dispersal mode rather than vegetation type constrained seed mass and seed storage allocation patterns in forest and savanna trees. We provide evidence that similar mechanisms are involved in seed storage of carbon and mineral nutrients across species.

Integration of skeletal traits in some passerines: impact (or the lack thereof) of body mass, phylogeny, diet and habitat.

Morphological integration of the bird skeleton is of great interest because it relates to issues of specialization, plasticity, and rate of evolutionary transformations of a skeleton as a whole and its anatomical regions. Despite growing interest, the integration and modularity of the skeleton of birds, in general, remain little studied. We evaluated the change of relative sizes and integration of shapes of skull, sternum and pelvis, and factors that influence the covariation of these regions among passerines. Results of both standard and phylogenetic reduced major axis showed that the relative lengths of the most studied skeletal traits were largely determined by body mass. The length of the skull scaled isometrically on body mass, and the lengths of both synsacrum and ilium showed positive allometry. Within the skull, beak length was positively allometric, whereas cranium length was negatively allometric with body mass. We found the presence of covariation between shapes of skull, sternum and pelvis using standard partial least squares (PLS) analysis and absence of covariation between most of these blocks using evolutionary PLS analysis on phylogenetic independent contrasts. Evolutionary integration is confirmed only for shapes of skull and pelvis (dorsal view).

Genome size and endopolyploidy evolution across the moss phylogeny.

BACKGROUND AND AIMS: Compared with other plant lineages, bryophytes have very small genomes with little variation across species, and high levels of endopolyploid nuclei. This study is the first analysis of moss genome evolution over a broad taxonomic sampling using phylogenetic comparative methods. We aim to determine whether genome size evolution is unidirectional as well as examine whether genome size and endopolyploidy are correlated in mosses. METHODS: Genome size and endoreduplication index (EI) estimates were newly generated using flow cytometry from moss samples collected in Canada. Phylogenetic relationships between moss species were reconstructed using GenBank sequence data and maximum likelihood methods. Additional 1C-values were compiled from the literature and genome size and EI were mapped onto the phylogeny to reconstruct ancestral character states, test for phylogenetic signal and perform phylogenetic independent contrasts. KEY RESULTS: Genome size and EI were obtained for over 50 moss taxa. New genome size estimates are reported for 33 moss species and new EIs are reported for 20 species. In combination with data from the literature, genome sizes were mapped onto a phylogeny for 173 moss species with this analysis, indicating that genome size evolution in mosses does not appear to be unidirectional. Significant phylogenetic signal was detected for genome size when evaluated across the phylogeny, whereas phylogenetic signal was not detected for EI. Genome size and EI were not found to be significantly correlated when using phylogenetically corrected values. CONCLUSIONS: Significant phylogenetic signal indicates closely related mosses have more similar genome sizes and EI values. This study supports that DNA content in mosses is defined by small genomes that are highly endopolyploid, suggesting strong selective pressure to maintain these features. Further research is needed to understand the functional significance of DNA content evolution in mosses.

Correlates of hybridization in plants.

Hybridization is a biological phenomenon increasingly recognized as an important evolutionary process in both plants and animals, as it is linked to speciation, radiation, extinction, range expansion and invasion, and allows for increased trait diversity in agricultural and horticultural systems. Estimates of hybridization frequency vary across taxonomic groups, but causes of this variation are unknown. Here, we ask on a global scale whether hybridization is linked to any of 11 traits related to plant life history, reproduction, genetic predisposition, and environment or opportunity. Given that hybridization is not evenly distributed across the plant tree of life, we use phylogenetic generalized least squares regression models and phylogenetic path analysis to detect statistical associations between hybridization and plant traits at both the family and genus levels. We find that perenniality and woodiness are each weakly associated with an increased frequency of hybridization in univariate analyses, but path analysis suggests that the direct linkage is between perenniality and increased hybridization (with woodiness having only an indirect relationship with hybridization via perenniality). Weak associations between higher rates of hybridization and higher outcrossing rates, abiotic pollination syndromes, vegetative reproductive modes, larger genomes, and less variable genome sizes are detectable in some cases but not others. We argue that correlational evidence at the global scale, such as that presented here, provides a robust framework for forming hypotheses to examine and test drivers of hybridization at a more mechanistic level.

Testing for correlation between traits under directional evolution.

Being confounding factors, directional trends are likely to make two quantitative traits appear as spuriously correlated. By determining the probability distributions of independent contrasts when traits evolve following Brownian motions with linear trends, we show that the standard independent contrasts can not be used to test for correlation in this situation. We propose a multiple regression approach which corrects the bias caused by directional evolution. We show that our approach is equivalent to performing a Phylogenetic Generalized Least Squares (PGLS) analysis with tip times as covariables by providing a new and more general proof of the equivalence between PGLS and independent contrasts methods. Our approach is assessed and compared with three previous correlation tests on data simulated in various situations and overall outperforms all the other methods. The approach is next illustrated on a real dataset to test for correlation between hominin cranial capacity and body mass.

Phylogenetic comparative methods: Harnessing the power of species diversity to investigate welfare issues in captive wild animals.

This paper reviews a way of investigating health and welfare problems in captive wild animals (e.g., those in zoos, aviaries, aquaria, or aquaculture systems) that has great potential, but to date has been little used: systematically comparing species with few or no health and welfare issues to those more prone to problems. Doing so empirically pinpoints species-typical welfare risk and protective factors (such as aspects of their natural behavioral biology): information which can then be used to help prevent or remedy problems by suggesting new ways to improve housing and husbandry, and by identifying species intrinsically best suited to captivity. We provide a detailed, step-by-step "how to" guide for researchers interested in using these techniques, including guidance on how to statistically control for the inherent similarities shared by related species: an important concern because simple, cross-species comparisons that do not do this may well fail to meet statistical assumptions of non-independence. The few relevant studies that have investigated captive wild animals' welfare problems using this method are described. Overall, such approaches reap value from the great number and diversity of species held in captivity (e.g., the many thousands of species held in zoos); can yield new insights from existing data and published results; render previously intractable welfare questions (such as "do birds need to fly?" or "do Carnivora need to hunt?") amenable to study; and generate evidence-based principles for integrating animal welfare into collection planning.

Long-legged bees make adaptive leaps: linking adaptation to coevolution in a plant-pollinator network.

Adaptation is evolution in response to natural selection. Hence, an adaptation is expected to originate simultaneously with the acquisition of a particular selective environment. Here we test whether long legs evolve in oil-collecting Rediviva bees when they come under selection by long-spurred, oil-secreting flowers. To quantify the selective environment, we drew a large network of the interactions between Rediviva species and oil-secreting plant species. The selective environment of each bee species was summarized as the average spur length of the interacting plant species weighted by interaction frequency. Using phylogenetically independent contrasts, we calculated divergence in selective environment and evolutionary divergence in leg length between sister species (and sister clades) of Rediviva We found that change in the selective environment explained 80% of evolutionary change in leg length, with change in body size contributing an additional 6% of uniquely explained variance. The result is one of four proposed steps in testing for plant-pollinator coevolution.

How bird clades diversify in response to climatic and geographic factors.

While the environmental correlates of global patterns in standing species richness are well understood, it is poorly known which environmental factors promote diversification (speciation minus extinction) in clades. We tested several hypotheses for how geographic and climatic variables should affect diversification using a large dataset of bird sister genera endemic to the New World. We found support for the area, evolutionary speed, environmental predictability and climatic stability hypotheses, but productivity and topographic complexity were rejected as explanations. Genera that had accumulated more species tend to occupy wider niche space, manifested both as occurrence over wider areas and in more habitats. Genera with geographic ranges that have remained more stable in response to glacial-interglacial changes in climate were also more species rich. Since many relevant explanatory variables vary latitudinally, it is crucial to control for latitude when testing alternative mechanistic explanations for geographic variation in diversification among clades.

Shedding light on the 'dark side' of phylogenetic comparative methods.

Phylogenetic comparative methods are becoming increasingly popular for investigating evolutionary patterns and processes. However, these methods are not infallible - they suffer from biases and make assumptions like all other statistical methods.Unfortunately, although these limitations are generally well known in the phylogenetic comparative methods community, they are often inadequately assessed in empirical studies leading to misinterpreted results and poor model fits. Here, we explore reasons for the communication gap dividing those developing new methods and those using them.We suggest that some important pieces of information are missing from the literature and that others are difficult to extract from long, technical papers. We also highlight problems with users jumping straight into software implementations of methods (e.g. in r) that may lack documentation on biases and assumptions that are mentioned in the original papers.To help solve these problems, we make a number of suggestions including providing blog posts or videos to explain new methods in less technical terms, encouraging reproducibility and code sharing, making wiki-style pages summarising the literature on popular methods, more careful consideration and testing of whether a method is appropriate for a given question/data set, increased collaboration, and a shift from publishing purely novel methods to publishing improvements to existing methods and ways of detecting biases or testing model fit. Many of these points are applicable across methods in ecology and evolution, not just phylogenetic comparative methods.

Vertebral shape and body elongation in Triturus newts.

Body elongation in vertebrates is often related to a lengthening of the vertebrae and an increase in their number. Changes in the number and shape of vertebrae are not necessarily linked. In tailed amphibians, a change in body shape is mostly associated with an increase in the number of trunk and tail vertebrae. Body elongation without a numerical change of vertebrae is rare. In Triturus aquatic salamanders body elongation is achieved by trunk elongation through an increase in the number of trunk vertebrae. We used computed microtomography and three-dimensional geometric morphometrics to document the size, shape and number of trunk vertebrae in seven Triturus species. The data suggest that body elongation has occurred more frequently than body shortening, possibly related to a more aquatic versus a more terrestrial locomotor style. Our results show that body elongation is achieved through an increase in the number of trunk vertebrae, and that interspecific differences in vertebral shape are correlated with this pattern of elongation. More gracile trunk vertebrae were found in the more elongated species. The shape differences are such that single trunk vertebrae can be used for the identification of species with a possible application in the identification of subfossil and fossil material.

Evolutionary divergence of leaf width and its correlates.

UNLABELLED: • PREMISE OF THE STUDY: The question why leaf dimensions vary so much between species has long puzzled ecologists. Presumably, variation arises from selective forces acting on leaf function but which selective forces and which leaf functions? This investigation assesses the consistency of divergence in plant traits and habitat variables in association with leaf width divergence in the flora of NSW, Australia.• METHODS: More than 80 traits and habitat variables were measured for 25 independent evolutionary divergence events (PICs). Each PIC was represented by two related plant species that had diverged substantially in leaf width. Outgroup species provided indications of the direction of divergence. Most PICs were within genus, so divergences represent relatively recent evolutionary events.• KEY RESULTS: No plant traits or habitat variables were 100% consistently associated with a divergence in leaf width, and surprisingly few diverged in a consistent direction significantly more than what might be expected by chance. This surprising lack of consistent divergence with leaf width contrasted with the result that many of these traits and habitat variables were correlated with leaf width across all species in our data set and in line with correlations reported from other studies. Subcategorizing PICs according to the probable direction of leaf width divergence did not improve consistency.• CONCLUSIONS: These results indicate that evolutionarily recent leaf width divergence events are not tightly tied to divergences in other leaf traits or in environmental situations, despite the broad correlations that have been observed across many species. Rather, cross species correlations are underpinned by earlier divergence events in the phylogeny.

Permutation tests for phylogenetic comparative analyses of high-dimensional shape data: what you shuffle matters.

Evaluating statistical trends in high-dimensional phenotypes poses challenges for comparative biologists, because the high-dimensionality of the trait data relative to the number of species can prohibit parametric tests from being computed. Recently, two comparative methods were proposed to circumvent this difficulty. One obtains phylogenetic independent contrasts for all variables, and statistically evaluates the linear model by permuting the phylogenetically independent contrasts (PICs) of the response data. The other uses a distance-based approach to obtain coefficients for generalized least squares models (D-PGLS), and subsequently permutes the original data to evaluate the model effects. Here, we show that permuting PICs is not equivalent to permuting the data prior to the analyses as in D-PGLS. We further explain why PICs are not the correct exchangeable units under the null hypothesis, and demonstrate that this misspecification of permutable units leads to inflated type I error rates of statistical tests. We then show that simply shuffling the original data and recalculating the independent contrasts with each iteration yields significance levels that correspond to those found using D-PGLS. Thus, while summary statistics from methods based on PICs and PGLS are the same, permuting PICs can lead to strikingly different inferential outcomes with respect to statistical and biological inferences.

Phylogeny suggests nondirectional and isometric evolution of sexual size dimorphism in argiopine spiders.

Sexual dimorphism describes substantial differences between male and female phenotypes. In spiders, sexual dimorphism research almost exclusively focuses on size, and recent studies have recovered steady evolutionary size increases in females, and independent evolutionary size changes in males. Their discordance is due to negative allometric size patterns caused by different selection pressures on male and female sizes (converse Rensch's rule). Here, we investigated macroevolutionary patterns of sexual size dimorphism (SSD) in Argiopinae, a global lineage of orb-weaving spiders with varying degrees of SSD. We devised a Bayesian and maximum-likelihood molecular species-level phylogeny, and then used it to reconstruct sex-specific size evolution, to examine general hypotheses and different models of size evolution, to test for sexual size coevolution, and to examine allometric patterns of SSD. Our results, revealing ancestral moderate sizes and SSD, failed to reject the Brownian motion model, which suggests a nondirectional size evolution. Contrary to predictions, male and female sizes were phylogenetically correlated, and SSD evolution was isometric. We interpret these results to question the classical explanations of female-biased SSD via fecundity, gravity, and differential mortality. In argiopines, SSD evolution may be driven by these or additional selection mechanisms, but perhaps at different phylogenetic scales.