The shape of mammalian phylogeny: patterns, processes and scales.

Mammalian phylogeny is far too asymmetric for all contemporaneous lineages to have had equal chances of diversifying. We consider this asymmetry or imbalance from four perspectives. First, we infer a minimal set of 'regime changes'-points at which net diversification rate has changed-identifying 15 significant radiations and 12 clades that may be 'downshifts'. We next show that mammalian phylogeny is similar in shape to a large set of published phylogenies of other vertebrate, arthropod and plant groups, suggesting that many clades may diversify under a largely shared set of 'rules'. Third, we simulate six simple macroevolutionary models, showing that those where speciation slows down as geographical or niche space is filled, produce more realistic phylogenies than do models involving key innovations. Lastly, an analysis of the spatial scaling of imbalance shows that the phylogeny of species within an assemblage, ecoregion or larger area always tends to be more unbalanced than expected from the phylogeny of species at the next more inclusive spatial scale. We conclude with a verbal model of mammalian macroevolution, which emphasizes the importance to diversification of accessing new regions of geographical or niche space.

The statistical mechanics of community assembly and species distribution.

• Theoretically, communities at or near their equilibrium species number resist entry of new species. Such 'biotic resistance' recently has been questioned because of successful entry of alien species into diverse natural communities. • Data on 10,409 naturalizations of 5350 plant species over 16 sites dispersed globally show exponential distributions both for species over sites and for sites over number of species shared. These exponentials signal a statistical mechanics of species distribution, assuming two conditions. First, species and sites are equivalent, either identical ('neutral') or so complex that the chance a species is in the right place at the right time is vanishingly small ('idiosyncratic'); the range of species and sites in our data disallows a neutral explanation. Secondly, the total number of naturalizations is fixed in any era by a 'regulator'. • Previous correlation of species naturalization rates with net primary productivity over time suggests that the regulator is related to productivity. • We conclude that biotic resistance is a moving ceiling, with resistance controlled by productivity. The general observation that the majority of species occur naturally at only a few sites, and only a few species occur at many sites, now has a quantitative (exponential) character, offering the study of species' distributions a previously unavailable rigor.

Phylogeny, niches, and relative abundance in natural communities.

Community structure refers to the number of species in a community and the pattern of distribution of individuals among those species. We use a novel way of representing community structure to show that abundance within closely related pairs of co-occurring tree species in a highly diverse Mexican forest is more equitable than is abundance within more distantly related pairs. This observation is at odds with the fundamental assumption of neutral models of community structure, i.e., that species are interchangeable. The observed patterns suggest niche apportionment, in which interaction is focused pairwise between congeners but falls away from the phylogenetic structure above the genus level. Thus niche processes may significantly affect community structure through regulating relative abundance in a substantial proportion of species, which in turn potentially enhances community stability. One such mechanism of stable coexistence has already been shown to be active in this forest.

Detecting non-Brownian trait evolution in adaptive radiations.

Many phylogenetic comparative methods that are currently widely used in the scientific literature assume a Brownian motion model for trait evolution, but the suitability of that model is rarely tested, and a number of important factors might affect whether this model is appropriate or not. For instance, we might expect evolutionary change in adaptive radiations to be driven by the availability of ecological niches. Such evolution has been shown to produce patterns of change that are different from those modelled by the Brownian process. We applied two tests for the assumption of Brownian motion that generally have high power to reject data generated under non-Brownian niche-filling models for the evolution of traits in adaptive radiations. As a case study, we used these tests to explore the evolution of feeding adaptations in two radiations of warblers. In one case, the patterns revealed do not accord with Brownian motion but show characteristics expected under certain niche-filling models.

Phylogenetically nested comparisons for testing correlates of species richness: a simulation study of continuous variables.

Explaining the uneven distribution of species among lineages is one of the oldest questions in evolution. Proposed correlations between biological traits and species diversity are routinely tested by making comparisons between phylogenetic sister clades. Several recent studies have used nested sister-clade comparisons to test hypotheses linking continuously varying traits, such as body size, with diversity. Evaluating the findings of these studies is complicated because they differ in the index of species richness difference used, the way in which trait differences were treated, and the statistical tests employed. In this paper, we use simulations to compare the performance of four species richness indices, two choices about the branch lengths used to estimate trait values for internal nodes and two statistical tests under a range of models of clade growth and character evolution. All four indices returned appropriate Type I error rates when the assumptions of the method were met and when branch lengths were set proportional to time. Only two of the indices were robust to the different evolutionary models and to different choices of branch lengths and statistical tests. These robust indices had comparable power under one nonnull scenario. Regression through the origin was consistently more powerful than the t-test, and the choice of branch lengths exerts a strong effect on both the validity and power. In the light of our simulations, we re-evaluate the findings of those who have previously used nested comparisons in the context of species richness. We provide a set of simple guidelines to maximize the performance of phylogenetically nested comparisons in tests of putative correlates of species richness.

Evolution: when females are brighter than males.

Females are usually considered to be more choosy than males when seeking a mating partner, resulting in the evolution of attractive males. When males are the limiting resource for receptive females, however, the females may become brightly coloured.

PHYLOGENIES WITHOUT FOSSILS.

Phylogenies that are reconstructed without fossil material often contain approximate dates for lineage splitting. For example, particular nodes on molecular phylogenies may be dated by known geographic events that caused lineages to split, thereby calibrating a molecular clock that is used to date other nodes. On the one hand, such phylogenies contain no information about lineages that have become extinct. On the other hand, they do provide a potentially useful testing ground for ideas about evolutionary processes. Here we first ask what such reconstructed phylogenies should be expected to look like under a birth-death process in which the birth and death parameters of lineages remain constant through time. We show that it is possible to estimate both the birth and death rates of lineages from the reconstructed phylogenies, even though they contain no explicit information about extinct lineages. We also show how such phylogenies can reveal mass extinctions and how their characteristic footprint can be distinguished from similar ones produced by density-dependent cladogenesis.

HOW MAMMALS PRODUCE LARGE-BRAINED OFFSPRING.

Two explanations for species differences in neonatal brain size in eutherian mammals relate the size of the brain at birth to maternal metabolic rate. Martin (1981, 1983) argued that maternal basal metabolic rate puts an upper bound on the mother's ability to supply energy to the fetus, thereby limiting neonatal brain size. Hofman (1983) proposed that gestation length in mammals is constrained by maternal metabolic rate, implying an indirect constraint on neonatal brain size. Since individuals of precocial species have much larger neonatal brain sizes and are gestated longer for a given maternal body size than individuals of altricial species, Martin's and Hofman's ideas also require that mothers of precocial offspring have higher metabolic rates for their body sizes than mothers of altricial offspring. Data on 116 mammal species from 13 orders show that neither neonatal brain size nor gestation length is correlated with maternal metabolic rate when maternal body-size effects are removed. For a given maternal size, there is no difference in metabolic rates between precocial and altricial species, despite a two-fold difference between them in average neonatal brain size. However, neonatal brain size is strongly correlated with gestation length and litter size, independently of maternal size and metabolic rate. Analyses conducted within orders replicated the findings for gestation length and suggested that neonatal brain size may be at best only weakly related to metabolic rate. Differences in neonatal brain size appear to have evolved primarily with species differences in gestation length and litter size but not with differences in metabolic rate; large-brained offspring are typically produced from litters of one that have been gestated for a long time relative to maternal size. We conclude that species differences in relative neonatal brain size reflect different life-history tactics rather than constraints imposed by metabolic rate.

LIFE HISTORY VARIATION IN PRIMATES.

Extensive variation in life-history patterns is documented across primate species. Variables included are gestation length, neonatal weight, litter size, age at weaning, age at sexual maturity, age at first breeding, longevity, and length of the estrous cycle. Species within genera and genera within subfamilies tend to be very similar on most measures, and about 85% of the variation remains when the subfamily is used as the level for statistical analysis. Variation in most life-history measures is highly correlated with variation in body size, and differences in body size are associated with differences in behavior and ecology. Allometric relationships between life-history variables and adult body weight are described; subfamily deviations from best-fit lines do not reveal strong correlations with behavior or ecology. However, for their body size, some subfamilies show consistently fast development across life-history stages while others are characteristically slow. One exception to the tendency for relative values to be positively correlated is brain growth: those primates with relatively large brains at birth have relatively less postnatal brain growth. Humans are a notable exception, with large brains at birth and high postnatal brain growth.