Disruption of trait-environment relationships in African megafauna occurred in the middle Pleistocene.

Mammalian megafauna have been critical to the functioning of Earth's biosphere for millions of years. However, since the Plio-Pleistocene, their biodiversity has declined concurrently with dramatic environmental change and hominin evolution. While these biodiversity declines are well-documented, their implications for the ecological function of megafaunal communities remain uncertain. Here, we adapt ecometric methods to evaluate whether the functional link between communities of herbivorous, eastern African megafauna and their environments (i.e., functional trait-environment relationships) was disrupted as biodiversity losses occurred over the past 7.4 Ma. Herbivore taxonomic and functional diversity began to decline during the Pliocene as open grassland habitats emerged, persisted, and expanded. In the mid-Pleistocene, grassland expansion intensified, and climates became more variable and arid. It was then that phylogenetic diversity declined, and the trait-environment relationships of herbivore communities shifted significantly. Our results divulge the varying implications of different losses in megafaunal biodiversity. Only the losses that occurred since the mid-Pleistocene were coincident with a disturbance to community ecological function. Prior diversity losses, conversely, occurred as the megafaunal species and trait pool narrowed towards those adapted to grassland environments.

Trophically integrated ecometric models as tools for demonstrating spatial and temporal functional changes in mammal communities.

We are in a modern biodiversity crisis that will restructure community compositions and ecological functions globally. Large mammals, important contributors to ecosystem function, have been affected directly by purposeful extermination and indirectly by climate and land-use changes, yet functional turnover is rarely assessed on a global scale using metrics based on functional traits. Using ecometrics, the study of functional trait distributions and functional turnover, we examine the relationship between vegetation cover and locomotor traits for artiodactyl and carnivoran communities. We show that the ability to detect a functional relationship is strengthened when locomotor traits of both primary consumers (artiodactyls, n = 157 species) and secondary consumers (carnivorans, n = 138 species) are combined into one trophically integrated ecometric model. Overall, locomotor traits of 81% of communities accurately estimate vegetation cover, establishing the advantage of trophically integrated ecometric models over single-group models (58 to 65% correct). We develop an innovative approach within the ecometrics framework, using ecometric anomalies to evaluate mismatches in model estimates and observed values and provide more nuance for understanding relationships between functional traits and vegetation cover. We apply our integrated model to five paleontological sites to illustrate mismatches in the past and today and to demonstrate the utility of the model for paleovegetation interpretations. Observed changes in community traits and their associated vegetations across space and over time demonstrate the strong, rapid effect of environmental filtering on community traits. Ultimately, our trophically integrated ecometric model captures the cascading interactions between taxa, traits, and changing environments.

A solution to the challenges of interdisciplinary aggregation and use of specimen-level trait data.

Understanding variation of traits within and among species through time and across space is central to many questions in biology. Many resources assemble species-level trait data, but the data and metadata underlying those trait measurements are often not reported. Here, we introduce FuTRES (Functional Trait Resource for Environmental Studies; pronounced few-tress), an online datastore and community resource for individual-level trait reporting that utilizes a semantic framework. FuTRES already stores millions of trait measurements for paleobiological, zooarchaeological, and modern specimens, with a current focus on mammals. We compare dynamically derived extant mammal species' body size measurements in FuTRES with summary values from other compilations, highlighting potential issues with simply reporting a single mean estimate. We then show that individual-level data improve estimates of body mass-including uncertainty-for zooarchaeological specimens. FuTRES facilitates trait data integration and discoverability, accelerating new research agendas, especially scaling from intra- to interspecific trait variability.

Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity.

Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 populations (77 species) of nonavian reptiles and amphibians. We test hypotheses of how thermoregulatory mode, environmental temperature, protective phenotypes, and pace of life history contribute to demographic aging. Controlling for phylogeny and body size, ectotherms display a higher diversity of aging rates compared with endotherms and include phylogenetically widespread evidence of negligible aging. Protective phenotypes and life-history strategies further explain macroevolutionary patterns of aging. Analyzing ectothermic tetrapods in a comparative context enhances our understanding of the evolution of aging.

Endocranial volume increases across captive generations in the endangered Mexican wolf.

Endangered animals in captivity may display reduced brain sizes due to captive conditions and limited genetic diversity. Captive diets, for example, may differ in nutrition and texture, altering cranial musculature and alleviating constraints on cranial shape development. Changes in brain size are associated with biological fitness, which may limit reintroduction success. Little is known about how changes in brain size progress in highly managed carnivoran populations and whether such traits are retained among reintroduced populations. Here, we measured the endocranial volume of preserved Mexican wolf skulls across captive generations and between captive, wild, and reintroduced populations and assessed endocranial volume dependence on inbreeding and cranial musculature. Endocranial volume increased across captive generations. However, we did not detect a difference among captive, wild, and reintroduced groups, perhaps due to the variability across captive generations. We did not find a relationship between endocranial volume and either inbreeding or cranial musculature, although the captive population displayed an increase in the cross-sectional area of the masseter muscle. We hypothesize that the increase in endocranial volume observed across captive generations may be related to the high-quality nutrition provided in captivity.

A Framework for Investigating Rules of Life by Establishing Zones of Influence.

The incredible complexity of biological processes across temporal and spatial scales hampers defining common underlying mechanisms driving the patterns of life. However, recent advances in sequencing, big data analysis, machine learning, and molecular dynamics simulation have renewed the hope and urgency of finding potential hidden rules of life. There currently exists no framework to develop such synoptic investigations. Some efforts aim to identify unifying rules of life across hierarchical levels of time, space, and biological organization, but not all phenomena occur across all the levels of these hierarchies. Instead of identifying the same parameters and rules across levels, we posit that each level of a temporal and spatial scale and each level of biological organization has unique parameters and rules that may or may not predict outcomes in neighboring levels. We define this neighborhood, or the set of levels, across which a rule functions as the zone of influence. Here, we introduce the zone of influence framework and explain using three examples: (a) randomness in biology, where we use a Poisson process to describe processes from protein dynamics to DNA mutations to gene expressions, (b) island biogeography, and (c) animal coloration. The zone of influence framework may enable researchers to identify which levels are worth investigating for a particular phenomenon and reframe the narrative of searching for a unifying rule of life to the investigation of how, when, and where various rules of life operate.

Comparison of environmental inference approaches for ecometric analyses: Using hypsodonty to estimate precipitation.

Ecometrics is the study of community-level functional trait-environment relationships. We use ecometric analyses to estimate paleoenvironment and to investigate community-level functional changes through time.We evaluate four methods that have been used or have the potential to be used in ecometric analyses for estimating paleoenvironment to determine whether there have been systematic differences in paleoenvironmental estimation due to choice of the estimation method. Specifically, we evaluated linear regression, polynomial regression, nearest neighbor, and maximum-likelihood methods to explore the predictive ability of the relationship for a well-known ecometric dataset of mammalian herbivore hypsodonty metrics (molar tooth crown to root height ratio) and annual precipitation. Each method was applied to 43 Pleistocene fossil sites and compared to annual precipitation from global climate models. Sites were categorized as glacial or interglacial, and paleoprecipitation estimates were compared to the appropriate model.Estimation methods produce results that are highly correlated with log precipitation and estimates from the other methods (p < 0.001). Differences between estimated precipitation and observed precipitation are not significantly different across the four methods, but maximum likelihood produces the most accurate estimates of precipitation. When applied to paleontological sites, paleoprecipitation estimates align more closely with glacial global climate models than with interglacial models regardless of the age of the site.Each method has constraints that are important to consider when designing ecometric analyses to avoid misinterpretations when ecometric relationships are applied to the paleontological record. We show interglacial fauna estimates of paleoprecipitation more closely match glacial global climate models. This is likely because of the anthropogenic effects on community reassembly in the Holocene.

Cranial morphology of captive mammals: a meta-analysis.

BACKGROUND: Captive facilities such as zoos are uniquely instrumental in conservation efforts. To fulfill their potential as bastions for conservation, zoos must preserve captive populations as appropriate proxies for their wild conspecifics; doing so will help to promote successful reintroduction efforts. Morphological changes within captive populations may be detrimental to the fitness of individual animals because these changes can influence functionality; thus, it is imperative to understand the breadth and depth of morphological changes occurring in captive populations. Here, we conduct a meta-analysis of scientific literature reporting comparisons of cranial measures between captive and wild populations of mammals. We investigate the pervasiveness of cranial differences and whether cranial morphological changes are associated with ecological covariates specific to individual species, such as trophic level, dietary breadth, and home range size. RESULTS: Cranial measures of skull length, skull width, and the ratio of skull length-to-width differed significantly between many captive and wild populations of mammals reported in the literature. Roughly half of captive populations differed from wild populations in at least one cranial measure, although the degree of changes varied. Carnivorous species with a limited dietary breadth displayed the most consistent changes associated with skull widening. Species with a more generalized diet displayed less morphological changes in captivity. CONCLUSIONS: Wild and captive populations of mammals differed in cranial morphology, but the nature and magnitude of their cranial differences varied considerably across taxa. Although changes in cranial morphology occur in captivity, specific changes cannot be generalized for all captive mammal populations. The nature of cranial changes in captivity may be specific to particular taxonomic groups; thus, it may be possible to establish expectations across smaller taxonomic units, or even disparate groups that utilize their cranial morphology in a similar way. Given that morphological changes occurring in captive environments like zoos have the potential to limit reintroduction success, our results call for a critical evaluation of current captive husbandry practices to prevent unnecessary morphological changes.

Spatial inequalities leave micropolitan areas and Indigenous populations underserved by informal STEM learning institutions.

Informal learning institutions (ILIs) create opportunities to increase public understanding of science and promote increased inclusion of groups underrepresented in Science, Technology, Engineering, and Math (STEM) careers but are not equally distributed across the United States. We explore geographic gaps in the ILI landscape and identify three groups of underserved counties based on the interaction between population density and poverty percentage. Among ILIs, National Park Service lands, biological field stations, and marine laboratories occur in areas with the fewest sites for informal learning opportunities and have the greatest potential to reach underserved populations, particularly in rural or high poverty counties. Most counties that are underserved by ILIs occur in the Great Plains, the southeast, and the northwest. Furthermore, these counties have higher Indigenous populations who are underrepresented in STEM careers. These unexpected geographic gaps represent opportunities for investments in ILI offerings through collaborations and expansion of existing resources.

Use of scalation landmarks in geometric morphometrics of squamate reptiles: a comment on homology.

Geometric morphometrics (GM) is a powerful analytical approach for evaluating phenotypic variation relevant to taxonomy and systematics, and as with any statistical methodology, requires adherence to fundamental assumptions for inferences to be strictly valid. An important consideration for GM is how landmark configurations, which represent sets of anatomical loci for evaluating shape variation through Cartesian coordinates, relate to underlying homology (Zelditch et al. 1995; Polly 2008). Perhaps more so than with traditional morphometrics, anatomical homology is a crucial assumption for GM because of the mathematical and biological interpretations associated with shape change depicted by deformation grids, such as the thin plate spline (Klingenberg 2008; Zelditch et al. 2012). GM approaches are often used to analyze shapes or outlines of structures, which are not necessarily related to common ancestry, and in this respect GM approaches that use linear semi-landmarks and related methods are particularly amenable to evaluating primary homology, or raw similarity between structures (De Pinna 1991; Palci Lee 2019). This relaxed interpretation of homology that focuses more on recognizable and repeatable landmarks is defensible so long as authors are clear regarding the purpose of the analyses and in defining their landmark configurations (Palci Lee 2019). Secondary homology, or similarity due to common ancestry, can also be represented with GM methods and is often assumed to be reflected in fixed Type 1 (juxtaposition of tissues) or Type 2 (self-evident geometry) landmarks (Bookstein 1991).

Phylogenetic structure of Holbrookia lacerata (Cope 1880) (Squamata: Phrynosomatidae): one species or two?

Species delimitation attempts to match species-level taxonomy with actual evolutionary lineages. Such taxonomic conclusions are typically, but not always, based on patterns of congruence across multiple data sources and methods of analyses. Here, we use this pluralistic approach to species delimitation to help resolve uncertainty in species boundaries of phrynosomatid sand lizards of the genus Holbrookia. Specifically, the Spot-tailed Earless Lizard (H. lacerata) was historically divided into a northern (H. l. lacerata) and southern (H. l. subcaudalis) subspecies based on differences in morphology and allopatry, but no research has been conducted evaluating genetic differences between these taxa. In this study, patterns in sequence data derived from two genes, one nuclear and one mitochondrial, for 66 individuals sampled across 18 counties in Texas revealed three strongly supported, reciprocally monophyletic lineages, each comprised of individuals from a single geographic region. Distinct genetic variation evident across two of these regions corresponds with differences in morphology, differences in environmental niche, and lines up with the presumed geographic barrier, the Balcones Escarpment, which is the historical subspecies boundary. The combined evidence from genetics, morphology and environmental niche is sufficient to consider these subspecies as distinct species with the lizards north of the Balcones Escarpment retaining the name Holbrookia lacerata, and those south of the Balcones Escarpment being designated as Holbrookia subcaudalis.

Modeling habitat suitability for chimpanzees (Pan troglodytes verus) in the Greater Nimba Landscape, Guinea, West Africa.

Tropical forests and the biodiversity within them are rapidly declining in the face of increasing human populations. Resource management and conservation of endangered species requires an understanding of how species perceive and respond to their environments. Species distribution modeling (SDM) is an appropriate tool for identifying conservation areas of concern and importance. In this study, SDM was used to identify areas of suitable chimpanzee (Pan troglodytes verus) habitat within the Greater Nimba Landscape, Guinea, West Africa. This location was ideal for investigating the effects of landscape structure on habitat suitability due to the topographic variation of the landscape and the Critically Endangered status of the Western chimpanzee. Additionally, this is the only mountainous, long-term chimpanzee study site and little is known about the effects of topography on chimpanzee behavior. Suitable habitat was predicted based on the location of direct and indirect signs of chimpanzee presence and the spatial distribution of 12 biophysical variables within the study area. Model performance was assessed by examining the area under the curve. The overall predictive performance of the model was 0.721. The variables most influencing habitat suitability were the normalized difference vegetation index (37.8%), elevation (27.3%), hierarchical slope position (11.5%), surface brightness (6.6%), and distance to rivers (5.4%). The final model highlighted the isolation and fragmentation of chimpanzee habitat within the Greater Nimba Landscape. Understanding the factors influencing chimpanzee habitat suitability, specifically the biophysical variables considered in this study, will greatly contribute to conservation efforts by providing quantitative habitat information and improving survey efficiency.

Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems.

Conservation of species and ecosystems is increasingly difficult because anthropogenic impacts are pervasive and accelerating. Under this rapid global change, maximizing conservation success requires a paradigm shift from maintaining ecosystems in idealized past states toward facilitating their adaptive and functional capacities, even as species ebb and flow individually. Developing effective strategies under this new paradigm will require deeper understanding of the long-term dynamics that govern ecosystem persistence and reconciliation of conflicts among approaches to conserving historical versus novel ecosystems. Integrating emerging information from conservation biology, paleobiology, and the Earth sciences is an important step forward on the path to success. Maintaining nature in all its aspects will also entail immediately addressing the overarching threats of growing human population, overconsumption, pollution, and climate change.

Including Fossils in Phylogenetic Climate Reconstructions: A Deep Time Perspective on the Climatic Niche Evolution and Diversification of Spiny Lizards (Sceloporus).

Fossils and other paleontological information can improve phylogenetic comparative method estimates of phenotypic evolution and generate hypotheses related to species diversification. Here, we use fossil information to calibrate ancestral reconstructions of suitable climate for Sceloporus lizards in North America. Integrating data from the fossil record, general circulation models of paleoclimate during the Miocene, climate envelope modeling, and phylogenetic comparative methods provides a geographically and temporally explicit species distribution model of Sceloporus-suitable habitat through time. We provide evidence to support the historic biogeographic hypothesis of Sceloporus diversification in warm North American deserts and suggest a relatively recent Sceloporus invasion into Mexico around 6 Ma. We use a physiological model to map extinction risk. We suggest that the number of hours of restriction to a thermal refuge limited Sceloporus from inhabiting Mexico until the climate cooled enough to provide suitable habitat at approximately 6 Ma. If the future climate returns to the hotter climates of the past, Mexico, the place of highest modern Sceloporus richness, will no longer provide suitable habitats for Sceloporus to survive and reproduce.

Limitations of climatic data for inferring species boundaries: insights from speckled rattlesnakes.

Phenotypes, DNA, and measures of ecological differences are widely used in species delimitation. Although rarely defined in such studies, ecological divergence is almost always approximated using multivariate climatic data associated with sets of specimens (i.e., the "climatic niche"); the justification for this approach is that species-specific climatic envelopes act as surrogates for physiological tolerances. Using identical statistical procedures, we evaluated the usefulness and validity of the climate-as-proxy assumption by comparing performance of genetic (nDNA SNPs and mitochondrial DNA), phenotypic, and climatic data for objective species delimitation in the speckled rattlesnake (Crotalus mitchellii) complex. Ordination and clustering patterns were largely congruent among intrinsic (heritable) traits (nDNA, mtDNA, phenotype), and discordance is explained by biological processes (e.g., ontogeny, hybridization). In contrast, climatic data did not produce biologically meaningful clusters that were congruent with any intrinsic dataset, but rather corresponded to regional differences in atmospheric circulation and climate, indicating an absence of inherent taxonomic signal in these data. Surrogating climate for physiological tolerances adds artificial weight to evidence of species boundaries, as these data are irrelevant for that purpose. Based on the evidence from congruent clustering of intrinsic datasets, we recommend that three subspecies of C. mitchellii be recognized as species: C. angelensis, C. mitchellii, and C. Pyrrhus.

Continuously growing rodent molars result from a predictable quantitative evolutionary change over 50 million years.

The fossil record is widely informative about evolution, but fossils are not systematically used to study the evolution of stem-cell-driven renewal. Here, we examined evolution of the continuous growth (hypselodonty) of rodent molar teeth, which is fuelled by the presence of dental stem cells. We studied occurrences of 3,500 North American rodent fossils, ranging from 50 million years ago (mya) to 2 mya. We examined changes in molar height to determine whether evolution of hypselodonty shows distinct patterns in the fossil record, and we found that hypselodont taxa emerged through intermediate forms of increasing crown height. Next, we designed a Markov simulation model, which replicated molar height increases throughout the Cenozoic and, moreover, evolution of hypselodonty. Thus, by extension, the retention of the adult stem cell niche appears to be a predictable quantitative rather than a stochastic qualitative process. Our analyses predict that hypselodonty will eventually become the dominant phenotype.

Evaluating the significance of paleophylogeographic species distribution models in reconstructing quaternary range-shifts of nearctic chelonians.

The climatic cycles of the Quaternary, during which global mean annual temperatures have regularly changed by 5-10°C, provide a special opportunity for studying the rate, magnitude, and effects of geographic responses to changing climates. During the Quaternary, high- and mid-latitude species were extirpated from regions that were covered by ice or otherwise became unsuitable, persisting in refugial retreats where the environment was compatible with their tolerances. In this study we combine modern geographic range data, phylogeny, Pleistocene paleoclimatic models, and isotopic records of changes in global mean annual temperature, to produce a temporally continuous model of geographic changes in potential habitat for 59 species of North American turtles over the past 320 Ka (three full glacial-interglacial cycles). These paleophylogeographic models indicate the areas where past climates were compatible with the modern ranges of the species and serve as hypotheses for how their geographic ranges would have changed in response to Quaternary climate cycles. We test these hypotheses against physiological, genetic, taxonomic and fossil evidence, and we then use them to measure the effects of Quaternary climate cycles on species distributions. Patterns of range expansion, contraction, and fragmentation in the models are strongly congruent with (i) phylogeographic differentiation; (ii) morphological variation; (iii) physiological tolerances; and (iv) intraspecific genetic variability. Modern species with significant interspecific differentiation have geographic ranges that strongly fluctuated and repeatedly fragmented throughout the Quaternary. Modern species with low genetic diversity have geographic distributions that were highly variable and at times exceedingly small in the past. Our results reveal the potential for paleophylogeographic models to (i) reconstruct past geographic range modifications, (ii) identify geographic processes that result in genetic bottlenecks; and (iii) predict threats due to anthropogenic climate change in the future.

Pleistocene climate, phylogeny, and climate envelope models: an integrative approach to better understand species' response to climate change.

Mean annual temperature reported by the Intergovernmental Panel on Climate Change increases at least 1.1°C to 6.4°C over the next 90 years. In context, a change in climate of 6°C is approximately the difference between the mean annual temperature of the Last Glacial Maximum (LGM) and our current warm interglacial. Species have been responding to changing climate throughout Earth's history and their previous biological responses can inform our expectations for future climate change. Here we synthesize geological evidence in the form of stable oxygen isotopes, general circulation paleoclimate models, species' evolutionary relatedness, and species' geographic distributions. We use the stable oxygen isotope record to develop a series of temporally high-resolution paleoclimate reconstructions spanning the Middle Pleistocene to Recent, which we use to map ancestral climatic envelope reconstructions for North American rattlesnakes. A simple linear interpolation between current climate and a general circulation paleoclimate model of the LGM using stable oxygen isotope ratios provides good estimates of paleoclimate at other time periods. We use geologically informed rates of change derived from these reconstructions to predict magnitudes and rates of change in species' suitable habitat over the next century. Our approach to modeling the past suitable habitat of species is general and can be adopted by others. We use multiple lines of evidence of past climate (isotopes and climate models), phylogenetic topology (to correct the models for long-term changes in the suitable habitat of a species), and the fossil record, however sparse, to cross check the models. Our models indicate the annual rate of displacement in a clade of rattlesnakes over the next century will be 2 to 3 orders of magnitude greater (430-2,420 m/yr) than it has been on average for the past 320 ky (2.3 m/yr).