Rapid change in mammalian eye shape is explained by activity pattern

The rate of morphological evolution along the branches of a phylogeny varies widely [1-6]. Although such rate variation is often assumed to reflect the strength of historical natural selection resulting in adaptation [7-14], this lacks empirical and analytical evidence. One way to demonstrate a relationship between branchwise rates and adaptation would be to show that rapid rates of evolution are linked with ecological shifts or key innovations. Here we test for this link by determining whether activity pattern – the time of day at which species are active – explains rapid bursts of evolutionary change in eye shape. Using modern approaches to identify shifts in the rate of morphological evolution [7, 13], we find that over 74% of rapid eye shape change during mammalian evolutionary history is directly explained by distinct selection pressures acting on nocturnal, cathemeral, and diurnal species. Our results reveal how ecological changes occurring along the branches of a phylogeny can manifest in subsequent changes in the rate of morphological evolution. Although selective pressures exerted by different activity patterns have acted uniformly across all mammals, we find differences in the rate of eye shape evolution among orders. The key to understanding this is in how ecology itself has evolved. We find heterogeneity in how activity pattern has evolved among mammals that ultimately led to differences in the rate of eye shape evolution among species. Our approach represents an exciting new way to pinpoint factors driving adaptation, enabling a clearer understanding of what factors drive the evolution of biological diversity

‘Residual diversity estimates’ do not correct for sampling bias in palaeodiversity data

1 It is widely accepted that the fossil record suffers from various sampling biases – diversity signals through time may partly or largely reflect the rock record – and many methods have been devised to deal with this problem. One widely used method, the ‘residual diversity’ method, uses residuals from a modelled relationship between palaeodiversity and sampling (sampling-driven diversity model) as ‘corrected’ diversity estimates, but the unorthodox way in which these residuals are generated presents serious statistical problems; the response and predictor variables are decoupled through independent sorting, rendering the new bivariate relationship meaningless. 2. Here, we use simple simulations to demonstrate the detrimental consequences of independent sorting, through assessing error rates and biases in regression model coefficients. 3. Regression models based on independently sorted data result in unacceptably high rates of incorrect and systematically, directionally biased estimates, when the true parameter values are known. The large number of recent papers that used the method are likely to have produced misleading results and their implications should be reassessed. 4. We note that the ‘residuals’ approach based on the sampling-driven diversity model cannot be used to ‘correct’ for sampling bias, and instead advocate the use of phylogenetic multiple regression models that can include various confounding factors, including sampling bias, while simultaneously accounting for statistical non-independence owing to shared ancestry. Evolutionary dynamics such as speciation are inherently a phylogenetic process, and only an explicitly phylogenetic approach will correctly model this process

Transitions between foot postures are associated with elevated rates of body size evolution in mammals

Terrestrial mammals have evolved various foot postures: flat-footed (plantigrady), tiptoed (digitigrady), and hooved (unguligrady) postures. Although the importance of foot posture on ecology and body size of mammalian species has been widely recognized, its evolutionary trajectory and influence on body size evolution across mammalian phylogeny remain untested. Taking a Bayesian phylogenetic approach combined with a comprehensive dataset of foot postures in 880 extant mammalian species, we investigated the evolutionary history of foot postures and rates of body size evolution, within the same posture and at transitions between postures. Our results show that the common ancestor of mammals was plantigrade, and transitions predominantly occurred only between plantigrady and digitigrady and between digitigrady and unguligrady. At the transitions between plantigrady and digitigrady and between digitigrady and unguligrady, rates of body size evolution are significantly elevated leading to the larger body masses of digitigrade species (∼1 kg) and unguligrade species (∼78 kg) compared with their respective ancestral postures [plantigrady (∼0.75 kg) and digitigrady]. Our results demonstrate the importance of foot postures on mammalian body size evolution and have implications for mammalian body size increase through time. In addition, we highlight a way forward for future studies that seek to integrate morphofunctional and macroevolutionary approaches

Dinosaurs in decline tens of millions of years before their final extinction

Whether dinosaurs were in a long-term decline or whether they were reigning strong right up to their final disappearance at the Cretaceous–Paleogene (K-Pg) mass extinction event 66 Mya has been debated for decades with no clear resolution. The dispute has continued unresolved because of a lack of statistical rigor and appropriate evolutionary framework. Here, for the first time to our knowledge, we apply a Bayesian phylogenetic approach to model the evolutionary dynamics of speciation and extinction through time in Mesozoic dinosaurs, properly taking account of previously ignored statistical violations. We find overwhelming support for a long-term decline across all dinosaurs and within all three dinosaurian subclades (Ornithischia, Sauropodomorpha, and Theropoda), where speciation rate slowed down through time and was ultimately exceeded by extinction rate tens of millions of years before the K-Pg boundary. The only exceptions to this general pattern are the morphologically specialized herbivores, the Hadrosauriformes and Ceratopsidae, which show rapid species proliferations throughout the Late Cretaceous instead. Our results highlight that, despite some heterogeneity in speciation dynamics, dinosaurs showed a marked reduction in their ability to replace extinct species with new ones, making them vulnerable to extinction and unable to respond quickly to and recover from the final catastrophic event

Adaptive evolution toward larger size in mammals

The notion that large body size confers some intrinsic advantage to biological species has been debated for centuries. Using a phylogenetic statistical approach that allows the rate of body size evolution to vary across a phylogeny, we find a long-term directional bias toward increasing size in the mammals. This pattern holds separately in 10 of 11 orders for which sufficient data are available and arises from a tendency for accelerated rates of evolution to produce increases, but not decreases, in size. On a branch-by-branch basis, increases in body size have been more than twice as likely as decreases, yielding what amounts to millions and millions of years of rapid and repeated increases in size away from the small ancestral mammal. These results are the first evidence, to our knowledge, from extant species that are compatible with Cope’s rule: the pattern of body size increase through time observed in the mammalian fossil record. We show that this pattern is unlikely to be explained by several nonadaptive mechanisms for increasing size and most likely represents repeated responses to new selective circumstances. By demonstrating that it is possible to uncover ancient evolutionary trends from a combination of a phylogeny and appropriate statistical models, we illustrate how data from extant species can complement paleontological accounts of evolutionary history, opening up new avenues of investigation for both

How body mass and lifestyle affect juvenile biomass production in placental mammals

In mammals, the mass-specific rate of biomass production during gestation and lactation, here called maternal productivity, has been shown to vary with body size and lifestyle. Metabolic theory predicts that post-weaning growth of offspring, here termed juvenile productivity, should be higher than maternal productivity, and juveniles of smaller species should be more productive than those of larger species. Furthermore because juveniles generally have similar lifestyles to their mothers, across species juvenile and maternal productivities should be correlated. We evaluated these predictions with data from 270 species of placental mammals in 14 taxonomic/lifestyle groups. All three predictions were supported. Lagomorphs, perissodactyls and artiodactyls were very productive both as juveniles and as mothers as expected from the abundance and reliability of their foods. Primates and bats were unproductive as juveniles and as mothers, as expected as an indirect consequence of their low predation risk and consequent low mortality. Our results point the way to a mechanistic explanation for the suite of correlated life-history traits that has been called the slow–fast continuum

Rapid decreases in relative testes mass among monogamous birds but not in other vertebrates

Larger testes produce more sperm and therefore improve reproductive success in the face of sperm competition. Adaptation to social mating systems with relatively high and low sperm competition are therefore likely to have driven changes in relative testes size in opposing directions. Here, we combine the largest vertebrate testes mass dataset ever collected with phylogenetic approaches for measuring rates of morphological evolution to provide the first quantitative evidence for how relative testes mass has changed over time. We detect explosive radiations of testes mass diversity distributed throughout the vertebrate tree of life: bursts of rapid change have been frequent during vertebrate evolutionary history. In socially monogamous birds, there have been repeated rapid reductions in relative testes mass. We see no such pattern in other monogamous vertebrates; the prevalence of monogamy in birds may have increased opportunities for investment in alternative behaviours and physiologies allowing reduced investment in expensive testes

Captive Rearing Program for Salmon River Chinook Salmon, 2002 Annual Report.

During 2002, the Idaho Department of Fish and Game continued to develop techniques to rear Chinook salmon Oncorhynchus tshawytscha to sexual maturity in captivity and to monitor their reproductive performance under natural conditions. Eyed-eggs were hydraulically collected from redds in the East Fork Salmon River (EFSR; N = 328) and the West Fork Yankee Fork Salmon River (WFYF; N = 308) to establish brood year 2002 culture cohorts. The eyed-eggs were incubated and reared at the Eagle Fish Hatchery, Eagle, Idaho (Eagle). Juveniles collected in 2000 were PIT and elastomer tagged and vaccinated against vibrio Vibrio spp. and bacterial kidney disease prior to being transferred to the NOAA Fisheries, Manchester Marine Experimental Station, Manchester, Washington (Manchester) for saltwater rearing through maturity. Smolt transfers included 203 individuals from the WFYF and 379 from the EFSR. Maturing fish transfers from Manchester to Eagle included 107 individuals from the LEM, 167 from the WFYF, and 82 from the EFSR. This was the second year maturing adults were held on chilled water at Eagle to test if water temperature manipulations could advance spawn timing. Adults from the LEM and WFYF were divided into chilled ({approx} 9 C) and ambient ({approx} 13.5 C) temperature groups while at Eagle. Forty-seven mature females from the LEM (19 chilled, 16 ambient, and 12 ambient not included in the temperature study) were spawned at Eagle with 42 males in 2002. Water temperature group was not shown to affect the spawn timing of these females, but males did mature earlier. Egg survival to the eyed stage averaged 66.5% and did not differ significantly between the temperature groups. Personnel from the Shoshone-Bannock Tribe placed a total of 47,977 eyed-eggs from these crosses in in-stream incubators. Mature adults (N = 215 including 56 precocial males) were released into the WFYF to evaluate their reproductive performance. After release, fish distributed themselves throughout the study section and displayed a progression of habitat associations and behavior consistent with progressing maturation and the onset of spawning. Twenty-six captive-reared females constructed 33 redds in the WFYF in 2002. Eighteen of these were hydraulically sampled, and eggs were collected from 17. The percentage of live eggs ranged from 0-100% and averaged 34.6%. No live eggs were found in redds spawned by brood year 1997 females. Expanding these results to the remaining redds gives an estimate of 22,900 eyed-eggs being produced by captive-reared fish in the WFYF. Additionally, 130 mature adults (including 41 precocial males) were released into the EFSR. Almost all of these fish moved out of the areas shoreline observers had access to, so no spawning behavior was observed. Radio-telemetry indicated that most of these fish initially moved downstream (although three females moved upstream as far as 7 km) and then held position

Phylogenetic non-independence in rates of trait evolution

Statistical non-independence of species’ biological traits is recognized in most traits under selection. Yet, whether or not the evolutionary rates of such biological traits are statistically non-independent remains to be tested. Here we test the hypothesis that phenotypic evolutionary rates are non-independent, i.e. contain phylogenetic signal, using empirical rates of evolution in three separate traits: body mass in mammals; beak shape in birds; and bite force in amniotes. Specifically, we test whether rates are non-independent throughout the evolutionary history of each tree. We find evidence for phylogenetic signal in evolutionary rates in all three case studies. While phylogenetic signal diminishes deeper in time, this is reflective of statistical power owing to small sample and effect sizes. When effect size is large, e.g., owing to the presence of fossil tips, we detect high phylogenetic signals even in deeper time slices. Thus, we recommend that rates be treated as being non-independent throughout the evolutionary history of the group of organisms under study, and any summaries or analyses of rates through time – including associations of rates with traits – need account for the undesired effects of shared ancestry