Characterizing the phylogenetic specialism-generalism spectrum of mammal parasites.

The distribution of parasites across mammalian hosts is complex and represents a differential ability or opportunity to infect different host species. Here, we take a macroecological approach to investigate factors influencing why some parasites show a tendency to infect species widely distributed in the host phylogeny (phylogenetic generalism) while others infect only closely related hosts. Using a database on over 1400 parasite species that have been documented to infect up to 69 terrestrial mammal host species, we characterize the phylogenetic generalism of parasites using standard effect sizes for three metrics: mean pairwise phylogenetic distance (PD), maximum PD and phylogenetic aggregation. We identify a trend towards phylogenetic specialism, though statistically host relatedness is most often equivalent to that expected from a random sample of host species. Bacteria and arthropod parasites are typically the most generalist, viruses and helminths exhibit intermediate generalism, and protozoa are on average the most specialist. While viruses and helminths have similar mean pairwise PD on average, the viruses exhibit higher variation as a group. Close-contact transmission is the transmission mode most associated with specialism. Most parasites exhibiting phylogenetic aggregation (associating with discrete groups of species dispersed across the host phylogeny) are helminths and viruses.

Parasite-mediated evolution of the functional part of the MHC in primates.

The major histocompatibility complex (MHC) is a key model of genetic polymorphism, but the mechanisms underlying its extreme variability are debated. Most hypotheses for MHC diversity focus on pathogen-driven selection and predict that MHC polymorphism evolves under the pressure of a diverse parasite fauna. Several studies reported that certain alleles offer protection against certain parasites, yet it remains unclear whether variation in parasite pressure more generally covaries with allelic diversity and rates of molecular evolution of MHC across species. We tested this prediction in a comparative study of 41 primate species. We characterized polymorphism of the exon 2 of DRB region of the MHC class II. Our phylogenetic analyses controlled for the potential effects of neutral mutation rate, population size, geographic origin and body mass and revealed that nematode species richness associates positively with nonsynonymous nucleotide substitution rate at the functional part of the molecule. We failed to find evidence for allelic diversity being strongly related to parasite species richness. Continental distribution was a strong predictor of both allelic diversity and substitution rate, with higher values in Malagasy and Neotropical primates. These results indicate that parasite pressure can influence the different estimates of MHC polymorphism, whereas geography plays an independent role in the natural history of MHC.

Sexual dimorphism in primate aerobic capacity: a phylogenetic test.

Male intrasexual competition should favour increased male physical prowess. This should in turn result in greater aerobic capacity in males than in females (i.e. sexual dimorphism) and a correlation between sexual dimorphism in aerobic capacity and the strength of sexual selection among species. However, physiological scaling laws predict that aerobic capacity should be lower per unit body mass in larger than in smaller animals, potentially reducing or reversing the sex difference and its association with measures of sexual selection. We used measures of haematocrit and red blood cell (RBC) counts from 45 species of primates to test four predictions related to sexual selection and body mass: (i) on average, males should have higher aerobic capacity than females, (ii) aerobic capacity should be higher in adult than juvenile males, (iii) aerobic capacity should increase with increasing sexual selection, but also that (iv) measures of aerobic capacity should co-vary negatively with body mass. For the first two predictions, we used a phylogenetic paired t-test developed for this study. We found support for predictions (i) and (ii). For prediction (iii), however, we found a negative correlation between the degree of sexual selection and aerobic capacity, which was opposite to our prediction. Prediction (iv) was generally supported. We also investigated whether substrate use, basal metabolic rate and agility influenced physiological measures of oxygen transport, but we found only weak evidence for a correlation between RBC count and agility.

Rapid evolution of social learning.

Culture is widely thought to be beneficial when social learning is less costly than individual learning and thus may explain the enormous ecological success of humans. Rogers (1988. Does biology constrain culture. Am. Anthropol. 90: 819-831) contradicted this common view by showing that the evolution of social learning does not necessarily increase the net benefits of learned behaviours in a variable environment. Using simulation experiments, we re-analysed extensions of Rogers' model after relaxing the assumption that genetic evolution is much slower than cultural evolution. Our results show that this assumption is crucial for Rogers' finding. For many parameter settings, genetic and cultural evolution occur on the same time scale, and feedback effects between genetic and cultural dynamics increase the net benefits. Thus, by avoiding the costs of individual learning, social learning can increase ecological success. Furthermore, we found that rapid evolution can limit the evolution of complex social learning strategies, which have been proposed to be widespread in animals.

Energetic constraints, not predation, influence the evolution of sleep patterning in mammals.

Mammalian sleep is composed of two distinct states - rapid-eye-movement (REM) and non-REM (NREM) sleep - that alternate in cycles over a sleep bout. The duration of these cycles varies extensively across mammalian species. Because the end of a sleep cycle is often followed by brief arousals to waking, a shorter sleep cycle has been proposed to function as an anti-predator strategy. Similarly, higher predation risk could explain why many species exhibit a polyphasic sleep pattern (division of sleep into several bouts per day), as having multiple sleep bouts avoids long periods of unconsciousness, potentially reducing vulnerability.Using phylogenetic comparative methods, we tested these predictions in mammals, and also investigated the relationships among sleep phasing, sleep-cycle length, sleep durations and body mass.Neither sleep-cycle length nor phasing of sleep was significantly associated with three different measures of predation risk, undermining the idea that they represent anti-predator adaptations.Polyphasic sleep was associated with small body size, shorter sleep cycles and longer sleep durations. The correlation with size may reflect energetic constraints: small animals need to feed more frequently, preventing them from consolidating sleep into a single bout. The reduced daily sleep quotas in monophasic species suggests that the consolidation of sleep into one bout per day may deliver the benefits of sleep more efficiently and, since early mammals were small-bodied and polyphasic, a more efficient monophasic sleep pattern could be a hitherto unrecognized advantage of larger size.

Why are some species more commonly afflicted by arthritis than others? A comparative study of spondyloarthropathy in primates and carnivores.

Spondyloarthropathy is a painful arthritic affliction of humans that also occurs in wild mammals. Important questions remain concerning the underlying causes of spondyloarthropathy in mammals, particularly regarding whether it is infectious in origin or driven by genetic predisposition and environmental stressors. Moreover, spondyloarthropathy has negative effects on host fitness, leading to potential conservation concerns if it impacts threatened species. Using a comparative data set on the prevalence of joint disease in 34 primate species and 100 carnivore species, we tested predictions involving the epidemiological correlates of spondyloarthropathy in wild mammals. Analyses revealed that 5.6% of primates and 3.6% of carnivores exhibited signs of spondyloarthropathy, with maximum incidence as high as 22% in great apes and 27% in bears. We tested whether prevalence of spondyloarthropathy increases with population density and group size, greater contact with soil, a slower host life history, increased ranging, dietary factors and body mass. We found general support for an effect of body mass, with larger bodied primates and carnivores exhibiting a higher prevalence of spondyloarthropathy. In addition, more threatened species experienced higher rates of spondyloarthropathy, with this association influenced by body mass and phylogeny. The effect of body mass could reflect that larger animals are exposed to more pathogens through greater consumption of resources, or that joints of larger bodied mammals experience greater biomechanical stresses, resulting in inflammation and activation of local joint infections.

Promiscuity and the primate immune system.

The behavioral and ecological factors involved in immune system evolution remain poorly explored. We present a phylogenetic analysis of white blood cell counts in primates to test three hypotheses related to disease risk: increases in risk are expected with group size or population density, exposure to soil-borne pathogens, and mating promiscuity. White blood cell counts were significantly greater in species where females have more mating partners, indicating that the risk of sexually transmitted disease is likely to be a major factor leading to systematic differences in the primate immune system.

Comparative tests of primate cognition: different scaling methods produce different results.

Although early comparative studies supported hypotheses that ecological demands selected for primate cognition, later work indicated that social demands were more important. One difference between earlier and later studies is that earlier studies scaled brain structures by (A) taking residuals from an interspecific regression of the brain structure in question on body mass, whereas later studies scaled them by (B) taking residuals from an interspecific regression of the brain structure in question on another brain structure or by (C) taking ratios of the brain structure in question to another brain structure. We conducted a series of comparative tests to explore the possibility that the different methods are responsible for the discrepancy between earlier and later studies. Specifically, we tested the ability of a social variable - group size - and an ecological variable - home range size - to explain variation in the non-V1 isocortex (isocortex minus primary visual cortex) when this structure was scaled with the three different methods. In multiple regression analysis, group size was a better predictor of the non-V1 isocortex with method (B). With methods (A) and (C), however, results were ambiguous: either home range size or group size explained more of the variation, depending on the inclusion of outliers, the use of independent contrasts, and whether home range size was scaled relative to body mass. We examine the three scaling methods and find no reasonable basis for preferring any of them. Hence, our results do not allow a distinction between social and ecological hypotheses. The general implications of our study are that (1) previous comparative studies are inconclusive and (2) further research is needed to develop a scaling method where relative measures of brain structure size are demonstrated to correspond with behavioral performance.

How quickly do brains catch up with bodies? A comparative method for detecting evolutionary lag.

A trait may be at odds with theoretical expectation because it is still in the process of responding to a recent selective force. Such a situation can be termed evolutionary lag. Although many cases of evolutionary lag have been suggested, almost all of the arguments have focused on trait fitness. An alternative approach is to examine the prediction that trait expression is a function of the time over which the trait could evolve. Here we present a phylogenetic comparative method for using this 'time' approach and we apply the method to a long-standing lag hypothesis: evolutionary changes in brain size lag behind evolutionary changes in body size. We tested the prediction in primates that brain mass contrast residuals, calculated from a regression of pairwise brain mass contrasts on positive pairwise body mass contrasts, are correlated with the time since the paired species diverged. Contrary to the brain size lag hypothesis, time since divergence was not significantly correlated with brain mass contrast residuals. We found the same result when we accounted for socioecology, used alternative body mass estimates and used male rather than female values. These tests do not support the brain size lag hypothesis. Therefore, body mass need not be viewed as a suspect variable in comparative neuroanatomical studies and relative brain size should not be used to infer recent evolutionary changes in body size.

Statistical analyses of developmental sequences: the craniofacial region in marsupial and placental mammals.

Heterochrony is most often thought to involve changes in the rate of development or maturation (rate changes). However, heterochrony can also involve changes in the timing of specific developmental events relative to other events (sequence changes). Sequence changes have received much less attention than have changes in developmental rates, in part because few methods exist for comparing developmental sequences. Here, we present two methods to statistically evaluate developmental sequence changes. First, Kendall's coefficient of concordance (W) is used to quantify overall similarity of developmental sequences in two or more groups of organisms, and second, ANOVA is used to identify the individual events that differ most in their relative developmental timing. Computer simulation is used to control for the nonindependence of species. We examine the sequence of developmental events in the craniofacial region of marsupial and placental mammals. We conclude that the most important differences in development in the two clades relate to the relative sequence of development of the central nervous system and somatic elements of the craniofacial region. The rationale behind the methods and their limitations are discussed, and the results from this study are compared with a previous analysis.

A simulation test of Smith's "Degrees of freedom" correction for comparative studies.

Computer simulation was used to test Smith's (1994) correction for phylogenetic nonindependence in comparative studies. Smith's method find effective N, which is computed using nested analysis of variance, and uses this value in place of observed N as the baseline degrees of freedom (df) for calculating statistical significance levels. If Smith's formula finds the correct df, distributions of computer-generated statistics from simulations with observed N nonindependent species should match theoretical distributions (from statistical tables) with the df based on effective N. The computer program developed to test Smith's method simulates character evolution down user-specified phylogenies. Parameters were systematically varied to discover their effects on Smith's method. In simulations in which the phylogeny and taxonomy were identical (tests of narrow-sense validity), Smith's method always gave conservative statistical results when the taxonomy had fewer than five levels. This conservative departure gave way to a liberal deviation in type I error rates in simulations using more than five taxonomic levels, except when species values were nearly independent. Reducing the number of taxonomic levels used in the analysis, and thereby eliminating available information regarding evolutionary relationships, also increased type I error rates (broad-sense validity), indicating that this may be inappropriate under conditions shown to have high type I error rates. However, the use of taxonomic categories over more accurate phylogenies did not create a liberal bias in all cases in the analysis performed here. The effect of correlated trait evolution was ambiguous but, relative to other parameters, negligible.

Correlation of carotid bruits and carotid atherosclerosis detected by B-mode real-time ultrasonography.

The extent of carotid atherosclerosis evaluated by B-mode real-time ultrasound and the presence of bruits established by carotid phonoangiography were determined in 1,107 patients. Unilateral bruit was associated with increased atherosclerosis compared with no bruit (p less than or equal to 0.0001). However, there was no association between laterality of the bruit and the degree of atherosclerosis (p = 0.66). There was marginal evidence that patients with bilateral bruits had more severe atherosclerosis than patients with unilateral bruit (p = 0.046). The relation between bruit and atherosclerosis categorized by B-mode ultrasound was not sufficient to reliably predict the presence or absence of disease in an individual patient, though the presence of a bruit should be viewed as a risk factor for, or an indicator of, increased risk of systemic atherosclerosis.

Three-dimensional transcranial Doppler blood flow mapping in patients with cerebrovascular disorders.

We investigated 60 patients with cerebrovascular disorders using a three-dimensional transcranial Doppler blood flow mapping system. A composite display of the circle of Willis is created with computer assistance, allowing accurate vessel identification and optimal data documentation of blood flow velocity and direction in the basal cerebral arteries. The basilar artery was insonated in every patient; the middle cerebral artery and the most distal internal carotid artery were found in 95% of the patients, the anterior cerebral artery in 85%, and the posterior cerebral artery in 84%. Insonation problems occurred predominantly in elderly women. Transcranial Doppler blood flow mapping showed an abnormal result in 23 of 60 patients (38%). An intracranial stenosis with greater than 50% diameter reduction or occlusion was found in 10 of 31 patients (32%) with completed stroke, reversible ischemic neurologic deficit, or transient ischemic attack. Collateral blood flow mechanisms could be demonstrated in patients with extracranial carotid artery occlusions. Intra-arterial cerebral angiography performed in 21 patients confirmed the transcranial Doppler blood flow mapping diagnosis in 19 (90.5%). In one patient an arteriovenous malformation diagnosed by transcranial Doppler blood flow mapping was confirmed by magnetic resonance imaging.