Homo heterogenus: Variability in early Pleistocene Homo environments.

To understand the ecological dominance of Homo sapiens, we need to investigate the origins of the plasticity that has enabled our colonization of the planet. We can approach this by exploring the variability of habitats to which different hominin populations have adapted over time. In this article, we draw upon and synthesize the current research on habitats of genus Homo during the early Pleistocene. We examined 121 published environmental reconstructions from 74 early Pleistocene sites or site phases to assess the balance of arguments in the research community. We found that, while grasslands and savannahs were prominent features of Homo habitats in the early Pleistocene, current research does not place early Pleistocene Homo, in any single environmental type, but in a wide variety of environments, ranging from open grasslands to forests. Our analysis also suggests that the first known dispersal of Homo out of Africa was accompanied by niche expansion.

Reconciling taxon senescence with the Red Queen's hypothesis.

In the fossil record, taxa exhibit a regular pattern of waxing and waning of occupancy, range or diversity between their origin and extinction. This pattern appears to contradict the law of constant extinction, which states that the probability of extinction in a given taxon is independent of that taxon's age. It is nevertheless well established for species, genera and higher taxa of terrestrial mammals, marine invertebrates, marine microorganisms, and recent Hawaiian clades of animals and plants. Here we show that the apparent contradiction between a stochastically constant extinction rate and the seemingly deterministic waxing and waning pattern of taxa disappears when we consider their peak of expansion rather than their final extinction. To a first approximation, we find that biotic drivers of evolution pertain mainly to the peak of taxon expansion, whereas abiotic drivers mainly apply to taxon extinction. The Red Queen's hypothesis, which emphasizes biotic interactions, was originally proposed as an explanation of the law of constant extinction. Much effort has since been devoted to determining how this hypothesis, emphasizing competition for resources, relates to the effects of environmental change. One proposed resolution is that biotic and abiotic processes operate at different scales. By focusing attention on taxon expansion rather than survival, we resolve an apparent contradiction between the seemingly deterministic waxing and waning patterns over time and the randomness of extinction that the Red Queen's hypothesis implies.

Do species factories exist? Detecting exceptional patterns of evolution in the mammalian fossil record.

A species factory refers to the source that gives rise to an exceptionally large number of species. However, what is it exactly: a place, a time or a combination of places, times and environmental conditions, remains unclear. Here we search for species factories computationally, for which we develop statistical approaches to detect origination, extinction and sorting hotspots in space and time in the fossil record. Using data on European Late Cenozoic mammals, we analyse where, how and how often species factories occur, and how they potentially relate to the dynamics of environmental conditions. We find that in the Early Miocene origination hotspots tend to be located in areas with relatively low estimated net primary productivity. Our pilot study shows that species first occurring in origination hotspots tend to have a longer average longevity and a larger geographical range than other species, thus emphasizing the evolutionary importance of the species factories.

Herbivore teeth predict climatic limits in Kenyan ecosystems.

A major focus in evolutionary biology is to understand how the evolution of organisms relates to changes in their physical environment. In the terrestrial realm, the interrelationships among climate, vegetation, and herbivores lie at the heart of this question. Here we introduce and test a scoring scheme for functional traits present on the worn surfaces of large mammalian herbivore teeth to capture their relationship to environmental conditions. We modeled local precipitation, temperature, primary productivity, and vegetation index as functions of dental traits of large mammal species in 13 national parks in Kenya over the past 60 y. We found that these dental traits can accurately estimate local climate and environment, even at small spatial scales within areas of relatively uniform climate (within two ecoregions), and that they predict limiting conditions better than average conditions. These findings demonstrate that the evolution of key functional properties of organisms may be more reflective of demands during recurring adverse episodes than under average conditions or during isolated severe events.

Paleoecology of the Serengeti during the Oldowan-Acheulean transition at Olduvai Gorge, Tanzania: The mammal and fish evidence.

Eight years of excavation work by the Olduvai Geochronology and Archaeology Project (OGAP) has produced a rich vertebrate fauna from several sites within Bed II, Olduvai Gorge, Tanzania. Study of these as well as recently re-organized collections from Mary Leakey's 1972 HWK EE excavations here provides a synthetic view of the faunal community of Olduvai during Middle Bed II at ∼1.7-1.4 Ma, an interval that captures the local transition from Oldowan to Acheulean technology. We expand the faunal list for this interval, name a new bovid species, clarify the evolution of several mammalian lineages, and record new local first and last appearances. Compositions of the fish and large mammal assemblages support previous indications for the dominance of open and seasonal grassland habitats at the margins of an alkaline lake. Fish diversity is low and dominated by cichlids, which indicates strongly saline conditions. The taphonomy of the fish assemblages supports reconstructions of fluctuating lake levels with mass die-offs in evaporating pools. The mammals are dominated by grazing bovids and equids. Habitats remained consistently dry and open throughout the entire Bed II sequence, with no major turnover or paleoecological changes taking place. Rather, wooded and wet habitats had already given way to drier and more open habitats by the top of Bed I, at 1.85-1.80 Ma. This ecological change is close to the age of the Oldowan-Acheulean transition in Kenya and Ethiopia, but precedes the local transition in Middle Bed II. The Middle Bed II large mammal community is much richer in species and includes a much larger number of large-bodied species (>300 kg) than the modern Serengeti. This reflects the severity of Pleistocene extinctions on African large mammals, with the loss of large species fitting a pattern typical of defaunation or 'downsizing' by human disturbance. However, trophic network (food web) analyses show that the Middle Bed II community was robust, and comparisons with the Serengeti community indicate that the fundamental structure of food webs remained intact despite Pleistocene extinctions. The presence of a generalized meat-eating hominin in the Middle Bed II community would have increased competition among carnivores and vulnerability among herbivores, but the high generality and interconnectedness of the Middle Bed II food web suggests this community was buffered against extinctions caused by trophic interactions.

Adaptive radiation of multituberculate mammals before the extinction of dinosaurs.

The Cretaceous-Paleogene mass extinction approximately 66 million years ago is conventionally thought to have been a turning point in mammalian evolution. Prior to that event and for the first two-thirds of their evolutionary history, mammals were mostly confined to roles as generalized, small-bodied, nocturnal insectivores, presumably under selection pressures from dinosaurs. Release from these pressures, by extinction of non-avian dinosaurs at the Cretaceous-Paleogene boundary, triggered ecological diversification of mammals. Although recent individual fossil discoveries have shown that some mammalian lineages diversified ecologically during the Mesozoic era, comprehensive ecological analyses of mammalian groups crossing the Cretaceous-Paleogene boundary are lacking. Such analyses are needed because diversification analyses of living taxa allow only indirect inferences of past ecosystems. Here we show that in arguably the most evolutionarily successful clade of Mesozoic mammals, the Multituberculata, an adaptive radiation began at least 20 million years before the extinction of non-avian dinosaurs and continued across the Cretaceous-Paleogene boundary. Disparity in dental complexity, which relates to the range of diets, rose sharply in step with generic richness and disparity in body size. Moreover, maximum dental complexity and body size demonstrate an adaptive shift towards increased herbivory. This dietary expansion tracked the ecological rise of angiosperms and suggests that the resources that were available to multituberculates were relatively unaffected by the Cretaceous-Paleogene mass extinction. Taken together, our results indicate that mammals were able to take advantage of new ecological opportunities in the Mesozoic and that at least some of these opportunities persisted through the Cretaceous-Paleogene mass extinction. Similar broad-scale ecomorphological inventories of other radiations may help to constrain the possible causes of mass extinctions.

Approaching a state shift in Earth's biosphere.

Localized ecological systems are known to shift abruptly and irreversibly from one state to another when they are forced across critical thresholds. Here we review evidence that the global ecosystem as a whole can react in the same way and is approaching a planetary-scale critical transition as a result of human influence. The plausibility of a planetary-scale 'tipping point' highlights the need to improve biological forecasting by detecting early warning signs of critical transitions on global as well as local scales, and by detecting feedbacks that promote such transitions. It is also necessary to address root causes of how humans are forcing biological changes.

The palaeoenvironment of the middle Miocene pliopithecid locality in Damiao, Inner Mongolia, China.

Damiao, Inner Mongolia, has three main fossil horizons representing the early, middle, and late Miocene. The middle Miocene locality DM01 is the only primate locality from the region and also represents the latest occurrence of pliopithecoids in northern China. The presence of pliopithecoid primates in central Asia after the middle Miocene climatic optimum seems to contradict the general trend of strengthening climatic zonality and increasing aridity. To investigate this enigma, we employ faunal similarity, ecometrics, and stable isotope analysis. Our results support previous inferences concerning the presence of locally humid environments within the increasingly arid surroundings that characterized central Asia. Hypsodonty, estimated mean annual precipitation (MAP), local sedimentology, and large mammal fossils suggest more humid and possibly more forested and wooded environments for the DM01 locality. We compared our results with the adjacent fossil-rich middle Miocene Tunggur localities. However, the small mammal fauna and isotope data are consistent with a mosaic of forest and grassland environment for all Damiao localities. Based on our results, Tunggur may have been too seasonal or not sufficiently humid for pliopithecids. This is supported by the higher mean hypsodonty and lower estimated MAP estimates, as well as slightly higher δ13C values. We suggest that DM01, the driest known Asian pliopithecid locality, may have been a more humid refugium within a generally drier regional context.

Modeling the Population-Level Processes of Biodiversity Gain and Loss at Geological Timescales.

The path of species diversification is commonly observed by inspecting the fossil record. Yet, how species diversity changes at geological timescales relate to lower-level processes remains poorly understood. Here we use mathematical models of spatially structured populations to show that natural selection and gradual environmental change give rise to discontinuous phenotype changes that can be connected to speciation and extinction at the macroevolutionary level. In our model, new phenotypes arise in the middle of the environmental gradient, while newly appearing environments are filled by existing phenotypes shifting their adaptive optima. Slow environmental change leads to loss of phenotypes in the middle of the extant environmental range, whereas fast change causes extinction at one extreme of the environmental range. We compared our model predictions against a well-known yet partially unexplained pattern of intense hoofed mammal diversification associated with grassland expansion during the Late Miocene. We additionally used the model outcomes to cast new insight into Cope's law of the unspecialized. Our general finding is that the rate of environmental change determines where generation and loss of diversity occur in the phenotypic and physical spaces.

Cope's Rule and the Universal Scaling Law of Ornament Complexity.

Luxuriant, bushy antlers, bizarre crests, and huge, twisting horns and tusks are conventionally understood as products of sexual selection. This view stems from both direct observation and from the empirical finding that the size of these structures grows faster than body size (i.e., ornament size shows positive allometry). We contend that the familiar evolutionary increase in the complexity of ornaments over time in many animal clades is decoupled from ornament size evolution. Increased body size comes with extended growth. Since growth scales to the quarter power of body size, we predicted that ornament complexity should scale according to the quarter power law as well, irrespective of the role of sexual selection in the evolution and function of the ornament. To test this hypothesis, we selected three clades (ammonites, deer, and ceratopsian dinosaurs) whose species bore ornaments that differ in terms of the importance of sexual selection to their evolution. We found that the exponent of the regression of ornament complexity to body size is the same for the three groups and is statistically indistinguishable from 0.25. We suggest that the evolution of ornament complexity is a by-product of Cope's rule. We argue that although sexual selection may control size in most ornaments, it does not influence their shape.

Co-occurrence of pliopithecoid and hominoid primates in the fossil record: An ecometric analysis.

Both pliopithecoid and hominoid primates were widely distributed throughout Eurasia during the Miocene but are known to have coexisted at only a few localities. It has been speculated that their different habitat preferences permitted only minimal overlap under special environmental conditions. Here we study the context for pliopithecoid and hominoid co-occurrence by assessing taxonomically-based palaeoecological diversity of associated fossil mammals and by direct ecometric analysis based on hypsodonty of mammalian herbivores. Our results show that pliopithecoids persistently inhabited more humid environments compared to the other primate groups studied, suggesting an inability to adapt to changing environmental conditions. The opportunity for hominoids and pliopithecoids to co-occur appears to have been restricted by niche conservatism in the latter group. Our study also indicates that direct ecometric analysis gives a better separation of the ecological preferences of these primate clades than do analyses of taxonomically-based community structure.

Adaptive dynamics on an environmental gradient that changes over a geological time-scale.

The standard adaptive dynamics framework assumes two timescales, i.e. fast population dynamics and slow evolutionary dynamics. We further assume a third timescale, which is even slower than the evolutionary timescale. We call this the geological timescale and we assume that slow climatic change occurs within this timescale. We study the evolution of our model population over this very slow geological timescale with bifurcation plots of the standard adaptive dynamics framework. The bifurcation parameter being varied describes the abiotic environment that changes over the geological timescale. We construct evolutionary trees over the geological timescale and observe both gradual phenotypic evolution and punctuated branching events. We concur with the established notion that branching of a monomorphic population on an environmental gradient only happens when the gradient is not too shallow and not too steep. However, we show that evolution within the habitat can produce polymorphic populations that inhabit steep gradients. What is necessary is that the environmental gradient at some point in time is such that the initial branching of the monomorphic population can occur. We also find that phenotypes adapted to environments in the middle of the existing environmental range are more likely to branch than phenotypes adapted to extreme environments.

The maximum rate of mammal evolution.

How fast can a mammal evolve from the size of a mouse to the size of an elephant? Achieving such a large transformation calls for major biological reorganization. Thus, the speed at which this occurs has important implications for extensive faunal changes, including adaptive radiations and recovery from mass extinctions. To quantify the pace of large-scale evolution we developed a metric, clade maximum rate, which represents the maximum evolutionary rate of a trait within a clade. We applied this metric to body mass evolution in mammals over the last 70 million years, during which multiple large evolutionary transitions occurred in oceans and on continents and islands. Our computations suggest that it took a minimum of 1.6, 5.1, and 10 million generations for terrestrial mammal mass to increase 100-, and 1,000-, and 5,000-fold, respectively. Values for whales were down to half the length (i.e., 1.1, 3, and 5 million generations), perhaps due to the reduced mechanical constraints of living in an aquatic environment. When differences in generation time are considered, we find an exponential increase in maximum mammal body mass during the 35 million years following the Cretaceous-Paleogene (K-Pg) extinction event. Our results also indicate a basic asymmetry in macroevolution: very large decreases (such as extreme insular dwarfism) can happen at more than 10 times the rate of increases. Our findings allow more rigorous comparisons of microevolutionary and macroevolutionary patterns and processes.

Patterns of maximum body size evolution in Cenozoic land mammals: eco-evolutionary processes and abiotic forcing.

There is accumulating evidence that macroevolutionary patterns of mammal evolution during the Cenozoic follow similar trajectories on different continents. This would suggest that such patterns are strongly determined by global abiotic factors, such as climate, or by basic eco-evolutionary processes such as filling of niches by specialization. The similarity of pattern would be expected to extend to the history of individual clades. Here, we investigate the temporal distribution of maximum size observed within individual orders globally and on separate continents. While the maximum size of individual orders of large land mammals show differences and comprise several families, the times at which orders reach their maximum size over time show strong congruence, peaking in the Middle Eocene, the Oligocene and the Plio-Pleistocene. The Eocene peak occurs when global temperature and land mammal diversity are high and is best explained as a result of niche expansion rather than abiotic forcing. Since the Eocene, there is a significant correlation between maximum size frequency and global temperature proxy. The Oligocene peak is not statistically significant and may in part be due to sampling issues. The peak in the Plio-Pleistocene occurs when global temperature and land mammal diversity are low, it is statistically the most robust one and it is best explained by global cooling. We conclude that the macroevolutionary patterns observed are a result of the interplay between eco-evolutionary processes and abiotic forcing.

Effects of allometry, productivity and lifestyle on rates and limits of body size evolution.

Body size affects nearly all aspects of organismal biology, so it is important to understand the constraints and dynamics of body size evolution. Despite empirical work on the macroevolution and macroecology of minimum and maximum size, there is little general quantitative theory on rates and limits of body size evolution. We present a general theory that integrates individual productivity, the lifestyle component of the slow-fast life-history continuum, and the allometric scaling of generation time to predict a clade's evolutionary rate and asymptotic maximum body size, and the shape of macroevolutionary trajectories during diversifying phases of size evolution. We evaluate this theory using data on the evolution of clade maximum body sizes in mammals during the Cenozoic. As predicted, clade evolutionary rates and asymptotic maximum sizes are larger in more productive clades (e.g. baleen whales), which represent the fast end of the slow-fast lifestyle continuum, and smaller in less productive clades (e.g. primates). The allometric scaling exponent for generation time fundamentally alters the shape of evolutionary trajectories, so allometric effects should be accounted for in models of phenotypic evolution and interpretations of macroevolutionary body size patterns. This work highlights the intimate interplay between the macroecological and macroevolutionary dynamics underlying the generation and maintenance of morphological diversity.

Exploring the mammalian sensory space: co-operations and trade-offs among senses.

The evolution of a particular sensory organ is often discussed with no consideration of the roles played by other senses. Here, we treat mammalian vision, olfaction and hearing as an interconnected whole, a three-dimensional sensory space, evolving in response to ecological challenges. Until now, there has been no quantitative method for estimating how much a particular animal invests in its different senses. We propose an anatomical measure based on sensory organ sizes. Dimensions of functional importance are defined and measured, and normalized in relation to animal mass. For 119 taxonomically and ecologically diverse species, we can define the position of the species in a three-dimensional sensory space. Thus, we can ask questions related to possible trade-off vs. co-operation among senses. More generally, our method allows morphologists to identify sensory organ combinations that are characteristic of particular ecological niches. After normalization for animal size, we note that arboreal mammals tend to have larger eyes and smaller noses than terrestrial mammals. On the other hand, we observe a strong correlation between eyes and ears, indicating that co-operation between vision and hearing is a general mammalian feature. For some groups of mammals we note a correlation, and possible co-operation between olfaction and whiskers.

High-level similarity of dentitions in carnivorans and rodents.

The study of mammalian evolution depends greatly on understanding the evolution of teeth and the relationship of tooth shape to diet. Links between gross tooth shape, function and diet have been proposed since antiquity, stretching from Aristotle to Cuvier, Owen and Osborn. So far, however, the possibilities for exhaustive, quantitative comparisons between greatly different tooth shapes have been limited. Cat teeth and mouse teeth, for example, are fundamentally distinct in shape and structure as a result of independent evolutionary change over tens of millions of years. There is difficulty in establishing homology between their tooth components or in summarizing their tooth shapes, yet both carnivorans and rodents possess a comparable spectrum of dietary specializations from animals to plants. Here we introduce homology-free techniques to measure the phenotypic complexity of the three-dimensional shape of tooth crowns. In our geographic information systems (GIS) analysis of 441 teeth from 81 species of carnivorans and rodents, we show that the surface complexity of tooth crowns directly reflects the foods they consume. Moreover, the absolute values of dental complexity for individual dietary classes correspond between carnivorans and rodents, illustrating a high-level similarity between overall tooth shapes despite a lack of low-level similarity of specific tooth components. These results suggest that scale-independent forces have determined the high-level dental shape in lineages that are widely divergent in size, ecology and life history. This link between diet and phenotype will be useful for inferring the ecology of extinct species and illustrates the potential of fast-throughput, high-level analysis of the phenotype.

Dental functional traits of mammals resolve productivity in terrestrial ecosystems past and present.

We have recently shown that rainfall, one of the main climatic determinants of terrestrial net primary productivity (NPP), can be robustly estimated from mean molar tooth crown height (hypsodonty) of mammalian herbivores. Here, we show that another functional trait of herbivore molar surfaces, longitudinal loph count, can be similarly used to extract reasonable estimates of rainfall but also of temperature, the other main climatic determinant of terrestrial NPP. Together, molar height and the number of longitudinal lophs explain 73 per cent of the global variation in terrestrial NPP today and resolve the main terrestrial biomes in bivariate space. We explain the functional interpretation of the relationships between dental function and climate variables in terms of long- and short-term demands. We also show how the spatially and temporally dense fossil record of terrestrial mammals can be used to investigate the relationship between biodiversity and productivity under changing climates in geological time. The placement of the fossil chronofaunas in biome space suggests that they most probably represent multiple palaeobiomes, at least some of which do not correspond directly to any biomes of today's world.

Distribution history and climatic controls of the Late Miocene Pikermian chronofauna.

The Late Miocene development of faunas and environments in western Eurasia is well known, but the climatic and environmental processes that controlled its details are incompletely understood. Here we map the rise and fall of the classic Pikermian fossil mammal chronofauna between 12 and 4.2 Ma, using genus-level faunal similarity between localities. To directly relate land mammal community evolution to environmental change, we use the hypsodonty paleoprecipitation proxy and paleoclimate modeling. The geographic distribution of faunal similarity and paleoprecipitation in successive timeslices shows the development of the open biome that favored the evolution and spread of the open-habitat adapted large mammal lineages. In the climate model run, this corresponds to a decrease in precipitation over its core area south of the Paratethys Sea. The process began in the latest Middle Miocene and climaxed in the medial Late Miocene, about 7-8 million years ago. The geographic range of the Pikermian chronofauna contracted in the latest Miocene, a time of increasing summer drought and regional differentiation of habitats in Eastern Europe and Southwestern Asia. Its demise at the Miocene-Pliocene boundary coincides with an environmental reversal toward increased humidity and forestation, changes inevitably detrimental to open-adapted, wide-ranging large mammals.