A global ecological signal of extinction risk in terrestrial vertebrates.

To determine the distribution and causes of extinction threat across functional groups of terrestrial vertebrates, we assembled an ecological trait data set for 18,016 species of terrestrial vertebrates and utilized phylogenetic comparative methods to test which categories of habitat association, mode of locomotion, and feeding mode best predicted extinction risk. We also examined the individual categories of the International Union for Conservation of Nature Red List extinction drivers (e.g., agriculture and logging) threatening each species and determined the greatest threats for each of the four terrestrial vertebrate groups. We then quantified the sum of extinction drivers threatening each species to provide a multistressor perspective on threat. Cave dwelling amphibians (p < 0.01), arboreal quadrupedal mammals (all of which are primates) (p < 0.01), aerial and scavenging birds (p < 0.01), and pedal (i.e., walking) squamates (p < 0.01) were all disproportionately threatened with extinction in comparison with the other assessed ecological traits. Across all threatened vertebrate species in the study, the most common risk factors were agriculture, threatening 4491 species, followed by logging, threatening 3187 species, and then invasive species and disease, threatening 2053 species. Species at higher risk of extinction were simultaneously at risk from a greater number of threat types. If left unabated, the disproportionate loss of species with certain functional traits and increasing anthropogenic pressures are likely to disrupt ecosystem functions globally. A shift in focus from species- to trait-centric conservation practices will allow for protection of at-risk functional diversity from regional to global scales.

Una Señal Ecológica Mundial del Riesgo de Extinción de los Vertebrados Terrestres Resumen Construimos un conjunto de datos de atributos ecológicos de 18,016 especies de vertebrados terrestres y utilizamos métodos de comparación filogenética para analizar cuáles categorías de asociación de hábitat, modo de locomoción y modo de alimentación predicen de mejor manera el riesgo de extinción. Lo anterior lo hicimos para determinar la distribución y las causas de las amenazas de extinción a lo largo de los grupos funcionales de vertebrados terrestres. También examinamos las categorías individuales de los factores de extinción (p. ej.: agricultura, tala de árboles) de la Lista Roja de la Unión Internacional para la Conservación de la Naturaleza que amenazan a cada especie y determinamos las principales amenazas para cada uno de los cuatro grupos de vertebrados terrestres. Después cuantificamos la suma de los factores de extinción que amenazan a cada especie para proporcionar una perspectiva de estresores múltiples sobre la amenaza. Los anfibios cavernícolas (p < 0.01), mamíferos arbóreos cuadrúpedos (todos son primates) (p < 0.01), aves aéreas y carroñeras (p < 0.01) y los escamados caminantes (p < 0.01) tuvieron una amenaza de extinción desproporcionada en comparación con los otros atributos ecológicos analizados. En todas las especies de vertebrados que estudiamos, los factores de riesgo más comunes fueron la agricultura, que amenaza a 4,491 especies, y la deforestación, que amenaza a 3,187 especies; le siguen las especies invasoras y las enfermedades, que juntas amenazan a 2,053 especies. Las especies con el mayor riesgo de extinción también se encontraban simultáneamente en riesgo por un mayor número de tipos de amenazas. Si esto se mantiene constante, la pérdida desproporcionada de especies con ciertos atributos funcionales y la creciente presión antropogénica probablemente alteren las funciones ecosistémicas a nivel mundial. Un cambio en el enfoque de las prácticas de conservación, de estar centradas en la especie a estar centradas en los atributos, permitirá la protección de la diversidad funcional en riesgo desde la escala regional hasta la global.

Statistical estimates of hominin origination and extinction dates: A case study examining the Australopithecus anamensis-afarensis lineage.

Reliable estimates of when hominin taxa originated and went extinct are central to addressing many paleoanthropological questions, including those relating to macroevolutionary patterns. The timing of hominin temporal ranges can be used to test chronological predictions generated from phylogenetic hypotheses. For example, hypotheses of phyletic ancestor-descendant relationships, based on morphological data, predict no temporal range overlap between the two taxa. However, a fossil taxon's observed temporal range is almost certainly underestimated due to the incompleteness of both the fossil record itself and its sampling, and this decreases the likelihood of observing temporal overlap. Here, we focus on a well-known and widely accepted early hominin lineage, Australopithecus anamensis-afarensis, and place 95% confidence intervals (CIs) on its origination and extinction dates. We do so to assess whether its temporal range is consistent with it being a phyletic descendant of Ardipithecus ramidus and/or a direct ancestor to the earliest claimed representative of Homo (i.e., Ledi-Geraru). We find that the last appearance of Ar. ramidus falls within the origination CI of Au. anamensis-afarensis, whereas the claimed first appearance of Homo postdates the extinction CI. These results are consistent with Homo evolving from Au. anamensis-afarensis, but temporal overlap between Ar. ramidus and Au. anamensis-afarensis cannot be rejected at this time. Though additional samples are needed, future research should extend our initial analyses to incorporate the uncertainties surrounding the range endpoints of Ar. ramidus and earliest Homo. Overall, our findings demonstrate the need for quantifying the uncertainty surrounding the appearances and disappearances of hominin taxa in order to better understand the timing of evolutionary events in our clade's history.

A quantitative formulation of biology's first law.

The zero-force evolutionary law (ZFEL) states that in evolutionary systems, in the absence of forces or constraints, diversity and complexity tend to increase. The reason is that diversity and complexity are both variance measures, and variances tend to increase spontaneously as random events accumulate. Here, we use random-walk models to quantify the ZFEL expectation, producing equations that give the probabilities of diversity or complexity increasing as a function of time, and that give the expected magnitude of the increase. We produce two sets of equations, one for the case in which variation occurs in discrete steps, the other for the case in which variation is continuous. The equations provide a way to decompose actual trajectories of diversity or complexity into two components, the portion due to the ZFEL and a remainder due to selection and constraint. Application of the equations is demonstrated using real and hypothetical data.

Do Bony Orbit Dimensions Predict Diel Activity Pattern in Sciurid Rodents?

Diel activity pattern (DAP) is a key aspect of an animal's ecology, but it is difficult to infer when behavior cannot be directly observed, as in the fossil record. Various anatomical correlates have therefore been used to attempt to classify DAP. Eyeball dimensions are good predictors of DAP because they relate directly to light sensitivity of the eye. Osteological characters, such as scleral ring dimensions, are also reliable proxies, but bony orbit dimensions alone have proven less reliable because soft tissues other than the eyeball can affect orbit size and shape. However, it would be useful if bony orbit dimensions could be used to determine DAP, particularly for mammals, which have no scleral ring, and nonmammalian synapsids, which infrequently preserve scleral rings. We investigated the possibility of predicting DAP in sciurids (Mammalia: Rodentia: Sciuridae) using orbit measurements and other cranial dimensions, and a variety of quantitative methods, including phylogenetic flexible discriminant analysis, classification trees, and logistic regression. The latter two methods do not require a priori assignment of DAP and therefore reflect the situation in a fossil data set. We find that although there are some interfering phylogenetic factors, nocturnal and non-nocturnal sciurids can be differentiated from one another with over 80% accuracy using all methods investigated here; attempts to differentiate crepuscular animals from nocturnal and diurnal species proved much less successful. Our results indicate that these analyses offer several viable options for predicting DAP in the fossil record, but such analyses should be conducted in a phylogenetic context whenever possible. Anat Rec, 301:1774-1787, 2018. © 2018 Wiley Periodicals, Inc.

Hierarchical complexity and the size limits of life.

Over the past 3.8 billion years, the maximum size of life has increased by approximately 18 orders of magnitude. Much of this increase is associated with two major evolutionary innovations: the evolution of eukaryotes from prokaryotic cells approximately 1.9 billion years ago (Ga), and multicellular life diversifying from unicellular ancestors approximately 0.6 Ga. However, the quantitative relationship between organismal size and structural complexity remains poorly documented. We assessed this relationship using a comprehensive dataset that includes organismal size and level of biological complexity for 11 172 extant genera. We find that the distributions of sizes within complexity levels are unimodal, whereas the aggregate distribution is multimodal. Moreover, both the mean size and the range of size occupied increases with each additional level of complexity. Increases in size range are non-symmetric: the maximum organismal size increases more than the minimum. The majority of the observed increase in organismal size over the history of life on the Earth is accounted for by two discrete jumps in complexity rather than evolutionary trends within levels of complexity. Our results provide quantitative support for an evolutionary expansion away from a minimal size constraint and suggest a fundamental rescaling of the constraints on minimal and maximal size as biological complexity increases.

Estimating times of extinction in the fossil record.

Because the fossil record is incomplete, the last fossil of a taxon is a biased estimate of its true time of extinction. Numerous methods have been developed in the palaeontology literature for estimating the true time of extinction using ages of fossil specimens. These methods, which typically give a confidence interval for estimating the true time of extinction, differ in the assumptions they make and the nature and amount of data they require. We review the literature on such methods and make some recommendations for future directions.

Animal evolution. Cope's rule in the evolution of marine animals.

Cope's rule proposes that animal lineages evolve toward larger body size over time. To test this hypothesis across all marine animals, we compiled a data set of body sizes for 17,208 genera of marine animals spanning the past 542 million years. Mean biovolume across genera has increased by a factor of 150 since the Cambrian, whereas minimum biovolume has decreased by less than a factor of 10, and maximum biovolume has increased by more than a factor of 100,000. Neutral drift from a small initial value cannot explain this pattern. Instead, most of the size increase reflects differential diversification across classes, indicating that the pattern does not reflect a simple scaling-up of widespread and persistent selection for larger size within populations.

Gradual assembly of avian body plan culminated in rapid rates of evolution across the dinosaur-bird transition.

The evolution of birds from theropod dinosaurs was one of the great evolutionary transitions in the history of life. The macroevolutionary tempo and mode of this transition is poorly studied, which is surprising because it may offer key insight into major questions in evolutionary biology, particularly whether the origins of evolutionary novelties or new ecological opportunities are associated with unusually elevated "bursts" of evolution. We present a comprehensive phylogeny placing birds within the context of theropod evolution and quantify rates of morphological evolution and changes in overall morphological disparity across the dinosaur-bird transition. Birds evolved significantly faster than other theropods, but they are indistinguishable from their closest relatives in morphospace. Our results demonstrate that the rise of birds was a complex process: birds are a continuum of millions of years of theropod evolution, and there was no great jump between nonbirds and birds in morphospace, but once the avian body plan was gradually assembled, birds experienced an early burst of rapid anatomical evolution. This suggests that high rates of morphological evolution after the development of a novel body plan may be a common feature of macroevolution, as first hypothesized by G.G. Simpson more than 60 years ago.

A shift in the long-term mode of foraminiferan size evolution caused by the end-Permian mass extinction.

Size is among the most important traits of any organism, yet the factors that control its evolution remain poorly understood. In this study, we investigate controls on the evolution of organismal size using a newly compiled database of nearly 25,000 foraminiferan species and subspecies spanning the past 400 million years. We find a transition in the pattern of foraminiferan size evolution from correlation with atmospheric pO2 during the Paleozoic (400-250 million years ago) to long-term stasis during the post-Paleozoic (250 million years ago to present). Thus, a dramatic shift in the evolutionary mode coincides with the most severe biotic catastrophe of the Phanerozoic (543 million years ago to present). Paleozoic tracking of pO2 was confined to Order Fusulinida, whereas Paleozoic lagenides, miliolids, and textulariids were best described by the stasis model. Stasis continued to best describe miliolids and textulariids during post-Paleozoic time, whereas random walk was the best supported mode for the other diverse orders. The shift in evolutionary dynamics thus appears to have resulted primarily from the selective elimination of fusulinids at the end of the Permian Period. These findings illustrate the potential for mass extinction to alter macroevolutionary dynamics for hundreds of millions of years.

Identifying heterogeneity in rates of morphological evolution: discrete character change in the evolution of lungfish (Sarcopterygii; Dipnoi).

Quantifying rates of morphological evolution is important in many macroevolutionary studies, and critical when assessing possible adaptive radiations and episodes of punctuated equilibrium in the fossil record. However, studies of morphological rates of change have lagged behind those on taxonomic diversification, and most authors have focused on continuous characters and quantifying patterns of morphological rates over time. Here, we provide a phylogenetic approach, using discrete characters and three statistical tests to determine points on a cladogram (branches or entire clades) that are characterized by significantly high or low rates of change. These methods include a randomization approach that identifies branches with significantly high rates and likelihood ratio tests that pinpoint either branches or clades that have significantly higher or lower rates than the pooled rate of the remainder of the tree. As a test case for these methods, we analyze a discrete character dataset of lungfish, which have long been regarded as "living fossils" due to an apparent slowdown in rates since the Devonian. We find that morphological rates are highly heterogeneous across the phylogeny and recover a general pattern of decreasing rates along the phylogenetic backbone toward living taxa, from the Devonian until the present. Compared with previous work, we are able to report a more nuanced picture of lungfish evolution using these new methods.

The evolutionary consequences of oxygenic photosynthesis: a body size perspective.

The high concentration of molecular oxygen in Earth's atmosphere is arguably the most conspicuous and geologically important signature of life. Earth's early atmosphere lacked oxygen; accumulation began after the evolution of oxygenic photosynthesis in cyanobacteria around 3.0-2.5 billion years ago (Gya). Concentrations of oxygen have since varied, first reaching near-modern values ~600 million years ago (Mya). These fluctuations have been hypothesized to constrain many biological patterns, among them the evolution of body size. Here, we review the state of knowledge relating oxygen availability to body size. Laboratory studies increasingly illuminate the mechanisms by which organisms can adapt physiologically to the variation in oxygen availability, but the extent to which these findings can be extrapolated to evolutionary timescales remains poorly understood. Experiments confirm that animal size is limited by experimental hypoxia, but show that plant vegetative growth is enhanced due to reduced photorespiration at lower O(2):CO(2). Field studies of size distributions across extant higher taxa and individual species in the modern provide qualitative support for a correlation between animal and protist size and oxygen availability, but few allow prediction of maximum or mean size from oxygen concentrations in unstudied regions. There is qualitative support for a link between oxygen availability and body size from the fossil record of protists and animals, but there have been few quantitative analyses confirming or refuting this impression. As oxygen transport limits the thickness or volume-to-surface area ratio-rather than mass or volume-predictions of maximum possible size cannot be constructed simply from metabolic rate and oxygen availability. Thus, it remains difficult to confirm that the largest representatives of fossil or living taxa are limited by oxygen transport rather than other factors. Despite the challenges of integrating findings from experiments on model organisms, comparative observations across living species, and fossil specimens spanning millions to billions of years, numerous tractable avenues of research could greatly improve quantitative constraints on the role of oxygen in the macroevolutionary history of organismal size.

Two-phase increase in the maximum size of life over 3.5 billion years reflects biological innovation and environmental opportunity.

The maximum size of organisms has increased enormously since the initial appearance of life >3.5 billion years ago (Gya), but the pattern and timing of this size increase is poorly known. Consequently, controls underlying the size spectrum of the global biota have been difficult to evaluate. Our period-level compilation of the largest known fossil organisms demonstrates that maximum size increased by 16 orders of magnitude since life first appeared in the fossil record. The great majority of the increase is accounted for by 2 discrete steps of approximately equal magnitude: the first in the middle of the Paleoproterozoic Era (approximately 1.9 Gya) and the second during the late Neoproterozoic and early Paleozoic eras (0.6-0.45 Gya). Each size step required a major innovation in organismal complexity--first the eukaryotic cell and later eukaryotic multicellularity. These size steps coincide with, or slightly postdate, increases in the concentration of atmospheric oxygen, suggesting latent evolutionary potential was realized soon after environmental limitations were removed.

Some problems with assessing Cope's Rule.

Cope's Rule states that the size of species tends to increase along an evolutionary lineage. A basic statistical framework is elucidated for testing Cope's Rule and some surprising complications are pointed out. If Cope's Rule is formulated in terms of mean size, then it is not invariant to the way in which size is measured. If Cope's Rule is formulated in terms of median size, then it is not invariant to the degree of separation between ancestral and descendant species. Some practical problems in assessing Cope's Rule are also described. These results have implications for the empirical assessment of Cope's Rule.

Trophic network models explain instability of Early Triassic terrestrial communities.

Studies of the end-Permian mass extinction have emphasized potential abiotic causes and their direct biotic effects. Less attention has been devoted to secondary extinctions resulting from ecological crises and the effect of community structure on such extinctions. Here we use a trophic network model that combines topological and dynamic approaches to simulate disruptions of primary productivity in palaeocommunities. We apply the model to Permian and Triassic communities of the Karoo Basin, South Africa, and show that while Permian communities bear no evidence of being especially susceptible to extinction, Early Triassic communities appear to have been inherently less stable. Much of the instability results from the faster post-extinction diversification of amphibian guilds relative to amniotes. The resulting communities differed fundamentally in structure from their Permian predecessors. Additionally, our results imply that changing community structures over time may explain long-term trends like declining rates of Phanerozoic background extinction.

Estimating the diversity of dinosaurs.

Despite current interest in estimating the diversity of fossil and extant groups, little effort has been devoted to estimating the diversity of dinosaurs. Here we estimate the diversity of nonavian dinosaurs at approximately 1,850 genera, including those that remain to be discovered. With 527 genera currently described, at least 71% of dinosaur genera thus remain unknown. Although known diversity declined in the last stage of the Cretaceous, estimated diversity was steady, suggesting that dinosaurs as a whole were not in decline in the 10 million years before their ultimate extinction. We also show that known diversity is biased by the availability of fossiliferous rock outcrop. Finally, by using a logistic model, we predict that 75% of discoverable genera will be known within 60-100 years and 90% within 100-140 years. Because of nonrandom factors affecting the process of fossil discovery (which preclude the possibility of computing realistic confidence bounds), our estimate of diversity is likely to be a lower bound.

Insulin resistance in the sisters of women with polycystic ovary syndrome: association with hyperandrogenemia rather than menstrual irregularity.

This study was performed to determine whether the sisters of women with polycystic ovary syndrome (PCOS) have evidence for insulin resistance. Three hundred and thirty-six women with PCOS, 307 sisters of these probands, and 47 control women were studied. The sisters were grouped by phenotypes: PCOS [hyperandrogenemia (HA) with chronic oligo- or amenorrhea, n = 39], HA with regular menses (n = 36), unaffected (UA; n = 122), and unknown (n = 110). The analyses were adjusted for age and body mass index. PCOS and HA sisters of women with PCOS had similar and significantly elevated fasting insulin levels (P = 0.001) as well as similar and significantly decreased fasting glucose/insulin ratios (P < 0.001) suggestive of insulin resistance compared with UA sisters and control women. Markers of insulin resistance were associated with hyperandrogenemia and not with menstrual irregularity. PCOS sisters also had decreased levels of SHBG (P = 0.02) suggestive of higher ambient insulin levels. PCOS sisters had increased levels of proinsulin (P = 0.04) compared with control women, which suggested pancreatic beta-cell dysfunction in this group of sisters. The magnitude of obesity also differed significantly among the groups of sisters. The PCOS sisters were significantly more obese than all the other groups, and the HA sisters were more obese than the UA sisters. We conclude that markers of insulin resistance are associated with hyperandrogenemia rather than menstrual irregularity in the sisters of women with PCOS. Menstrual irregularity may be related to the magnitude of insulin sensitivity or insulin secretion or to other factors associated with obesity.

Elevated dehydroepiandrosterone sulfate levels as the reproductive phenotype in the brothers of women with polycystic ovary syndrome.

There is an inherited susceptibility to polycystic ovary syndrome (PCOS). Some investigators have suggested that premature male-pattern balding is a male phenotype in PCOS families, but this remains controversial. We recently reported evidence for an autosomal monogenic abnormality in ovarian and adrenal steroidogenesis in the sisters of women with PCOS. We performed this study to determine whether we could identify a clinical or biochemical phenotype in the brothers of women with PCOS. One hundred nineteen brothers of 87 unrelated women with PCOS and 68 weight- and ethnicity-comparable unrelated control men were examined and had fasting blood samples obtained. The odds of balding (Hamilton score > or = V) did not differ in the brothers of PCOS women compared with control men. Brothers of women with PCOS had significantly elevated dehydroepiandrosterone sulfate (DHEAS) levels [brothers 3035 +/- 1132 ng/ml (mean +/- SD) vs. control men 2494 +/- 1172 ng/ml; P < 0.05]. There was a significant positive linear relationship between DHEAS levels in PCOS probands and their brothers (r = 0.35; P = 0.001). There was no significant bimodal distribution in DHEAS levels, and there were no significant differences in other parameters in brothers of PCOS women with high DHEAS levels compared with those with low DHEAS levels. There is familial clustering of elevated DHEAS levels in the brothers of women with PCOS, suggesting that this is a genetic trait. This might reflect the same underlying defect in steroidogenesis that we found in the sisters of women with PCOS. Balding was not increased in the brothers of women with PCOS. We conclude that there is a biochemical reproductive endocrine phenotype in men in PCOS families.