Many-to-many mapping: A simulation study of how the number of traits and tasks affect the evolution of form and function.

Many-to-many mapping of form-to-function posits that multiple morphological and physiological traits affect the performance of multiple tasks in an organism, and that redundancy and multitasking occur simultaneously to shape the evolution of an organism's phenotype. Many-to-many mapping is expected to be ubiquitous in nature, yet little is known about how it influences the evolution of organismal phenotype. The F-matrix is a powerful tool to study these issues because it describes how multiple traits affect multiple tasks. We undertook a simulation study using the F-matrix to test how the number of traits and the number of tasks affect trait integration and evolvability, as well as the relationships among tasks. We found that as the number of traits and/or tasks increases, the relationships between the tasks and the integration between the traits become weaker, and that the evolvability of the traits increases, all resulting in a system that is freer to evolve. We also found that as the number of traits increases, performance tradeoffs tend to become weaker, but only to a point. Our work shows that it is important to consider not only multiple traits, but also the multitude of tasks that those traits carry out when studying form-function relationships. We suggest that evolution of these relationships follows functional lines of least resistance, which are less defined in more complex systems, resulting in a mechanism for diversification.

Coordinating tiny limbs and long bodies: Geometric mechanics of lizard terrestrial swimming.

Although typically possessing four limbs and short bodies, lizards have evolved diverse morphologies, including elongate trunks with tiny limbs. Such forms are hypothesized to aid locomotion in cluttered/fossorial environments but propulsion mechanisms (e.g., the use of body and/or limbs to interact with substrates) and potential body/limb coordination remain unstudied. Here, we use biological experiments, a geometric theory of locomotion, and robophysical models to investigate body-limb coordination in diverse lizards. Locomotor field studies in short-limbed, elongate lizards (Brachymeles and Lerista) and laboratory studies of fully limbed lizards (Uma scoparia and Sceloporus olivaceus) and a snake (Chionactis occipitalis) reveal that body-wave dynamics can be described by a combination of standing and traveling waves; the ratio of the amplitudes of these components is inversely related to the degree of limb reduction and body elongation. The geometric theory (which replaces laborious calculation with diagrams) helps explain our observations, predicting that the advantage of traveling-wave body undulations (compared with a standing wave) emerges when the dominant thrust-generation mechanism arises from the body rather than the limbs and reveals that such soil-dwelling lizards propel via "terrestrial swimming" like sand-swimming lizards and snakes. We test our hypothesis by inducing the use of traveling waves in stereotyped lizards via modulating the ground-penetration resistance. Study of a limbed/undulatory robophysical model demonstrates that a traveling wave is beneficial when propulsion is generated by body-environment interaction. Our models could be valuable in understanding functional constraints on the evolutionary processes of elongation and limb reduction as well as advancing robot designs.

Performance and Kinematic Differences Between Terrestrial and Aquatic Running in Anolis Sagrei.

Many animals frequently transition between different media while navigating their heterogeneous environments. These media vary in compliance, moisture content, and other characteristics that affect their physical properties. As a result, animals may need to alter their kinematics to adapt to potential changes in media while maintaining performance during predator escape and foraging. Due to its fluid nature, water is highly compliant, and although usually associated with swimming, water running has evolved in a variety of animals ranging from insects to mammals. While the best studied large water runners are the bipedal basilisk lizards (Basiliscus spp.), other lizards have also been observed to run across the surface of water, namely, Hemidactylus platyurus, a house gecko, and in this study, Anolis sagrei, the brown anole. Unlike the basilisk lizard, the primarily arboreal Anolis sagrei is not adapted for water running. Moreover, water running in A. sagrei, similar to that of the house gecko, was primarily quadrupedal. Here, we tested for performance and kinematic differences between aquatic and terrestrial running and if the variance in performance and kinematic variables differed between the two media. We found no difference in average and maximum velocity between running on land and water. We also found that Anolis sagrei had higher hindlimb stride frequencies, decreased duty factor, and shorter stride lengths on water, as well as more erect postures. Finally, we found that most kinematics did not differ in variance between the two media, but of those that were different, almost all were more variable during terrestrial running. Our findings show that animals may be capable of specialized modes of locomotion, even if they are not obviously adapted for them, and that they may do this by modulating their kinematics to facilitate locomotion through novel environments.

County-level societal predictors of COVID-19 cases and deaths changed through time in the United States: A longitudinal ecological study.

People of different racial/ethnic backgrounds, demographics, health, and socioeconomic characteristics have experienced disproportionate rates of infection and death due to COVID-19. This study tests if and how county-level rates of infection and death have changed in relation to societal county characteristics through time as the pandemic progressed. This longitudinal study sampled monthly county-level COVID-19 case and death data per 100,000 residents from April 2020 to March 2022, and studied the relationships of these variables with racial/ethnic, demographic, health, and socioeconomic characteristics for 3125 or 97.0% of U.S. counties, accounting for 96.4% of the U.S. population. The association of all county-level characteristics with COVID-19 case and death rates changed significantly through time, and showed different patterns. For example, counties with higher population proportions of Black, Native American, foreign-born non-citizen, elderly residents, households in poverty, or higher income inequality suffered disproportionately higher COVID-19 case and death rates at the beginning of the pandemic, followed by reversed, attenuated or fluctuating patterns, depending on the variable. Patterns for counties with higher White versus Black population proportions showed somewhat inverse patterns. Counties with higher female population proportions initially had lower case rates but higher death rates, and case and death rates become more coupled and fluctuated later in the pandemic. Counties with higher population densities had fluctuating case and death rates, with peaks coinciding with new variants of COVID-19. Counties with a greater proportion of university-educated residents had lower case and death rates throughout the pandemic, although the strength of this relationship fluctuated through time. This research clearly shows that how different segments of society are affected by a pandemic changes through time. Therefore, targeted policies and interventions that change as a pandemic unfolds are necessary to mitigate its disproportionate effects on vulnerable populations, particularly during the first six months of a pandemic.

Linking ecomechanical models and functional traits to understand phenotypic diversity.

Physical principles and laws determine the set of possible organismal phenotypes. Constraints arising from development, the environment, and evolutionary history then yield workable, integrated phenotypes. We propose a theoretical and practical framework that considers the role of changing environments. This 'ecomechanical approach' integrates functional organismal traits with the ecological variables. This approach informs our ability to predict species shifts in survival and distribution and provides critical insights into phenotypic diversity. We outline how to use the ecomechanical paradigm using drag-induced bending in trees as an example. Our approach can be incorporated into existing research and help build interdisciplinary bridges. Finally, we identify key factors needed for mass data collection, analysis, and the dissemination of models relevant to this framework.

How head shape and substrate particle size affect fossorial locomotion in lizards.

Granular substrates ranging from silt to gravel cover much of the Earth's land area, providing an important habitat for fossorial animals. Many of these animals use their heads to penetrate the substrate. Although there is considerable variation in head shape, how head shape affects fossorial locomotor performance in different granular substrates is poorly understood. Here, head shape variation for 152 species of fossorial lizards was quantified for head diameter, slope and pointiness of the snout. The force needed to penetrate different substrates was measured using 28 physical models spanning this evolved variation. Ten substrates were considered, ranging in particle size from 0.025 to 4 mm in diameter and consisting of spherical or angular particles. Head shape evolved in a weakly correlated manner, with snouts that were gently sloped being blunter. There were also significant clade differences in head shape among fossorial lizards. Experiments with physical models showed that as head diameter increased, absolute penetration force increased but force normalized by cross-sectional area decreased. Penetration force decreased for snouts that tapered more gradually and were pointier. Larger and angular particles required higher penetration forces, although intermediate size spherical particles, consistent with coarse sand, required the lowest force. Particle size and head diameter effect were largest, indicating that fossorial burrowers should evolve narrow heads and bodies, and select relatively fine particles. However, variation in evolved head shapes and recorded penetration forces suggests that kinematics of fossorial movement are likely an important factor in explaining evolved diversity.

Locomotion and palaeoclimate explain the re-evolution of quadrupedal body form in Brachymeles lizards.

Evolutionary reversals, including re-evolution of lost structures, are commonly found in phylogenetic studies. However, we lack an understanding of how these reversals happen mechanistically. A snake-like body form has evolved many times in vertebrates, and occasionally a quadrupedal form has re-evolved, including in Brachymeles lizards. We use body form and locomotion data for species ranging from snake-like to quadrupedal to address how a quadrupedal form could re-evolve. We show that large, quadrupedal species are faster at burying and surface locomotion than snake-like species, indicating a lack of expected performance trade-off between these modes of locomotion. Species with limbs use them while burying, suggesting that limbs are useful for burying in wet, packed substrates. Palaeoclimatological data suggest that Brachymeles originally evolved a snake-like form under a drier climate probably with looser soil in which it was easier to dig. The quadrupedal clade evolved as the climate became humid, where limbs and large size facilitated fossorial locomotion in packed soils.

Using 3D-digital photogrammetry to examine scaling of the body axis in burrowing skinks.

Three-dimensional (3D) modeling techniques have been increasingly utilized across disciplines for the visualization and analysis of complex structures. We employ 3D-digital photogrammetry for understanding the scaling of the body axis of 12 species of scincid lizards in the genus Brachymeles. These skinks represent a diverse radiation which shows tremendous variation in body size and degree of axial elongation. Because of the complex nature of the body axis, 3D-methods are important for understanding how the body axis evolves. 3D-digital photogrammetry presents a flexible, inexpensive, and portable system for the reconstruction of biological forms. As body size increased among species, the cross-sectional area and circumference of the head and other portions of the body axis increased isometrically, which indicates that species of differing sizes possess proportionally similar head and body shapes. These results suggest that there are no substantial head and body shape changes with body size among the sampled species, but further comparative studies with larger sample sizes and functional studies of size and morphology effects on burrowing or above-ground locomotion are needed.

Convergent Evolution of Elongate Forms in Craniates and of Locomotion in Elongate Squamate Reptiles.

Synopsis Elongate, snake- or eel-like, body forms have evolved convergently many times in most major lineages of vertebrates. Despite studies of various clades with elongate species, we still lack an understanding of their evolutionary dynamics and distribution on the vertebrate tree of life. We also do not know whether this convergence in body form coincides with convergence at other biological levels. Here, we present the first craniate-wide analysis of how many times elongate body forms have evolved, as well as rates of its evolution and reversion to a non-elongate form. We then focus on five convergently elongate squamate species and test if they converged in vertebral number and shape, as well as their locomotor performance and kinematics. We compared each elongate species to closely related quadrupedal species and determined whether the direction of vertebral or locomotor change matched in each case. The five lineages examined are obscure species from remote locations, providing a valuable glimpse into their biology. They are the skink lizards Brachymeles lukbani, Lerista praepedita, and Isopachys anguinoides, the basal squamate Dibamus novaeguineae, and the basal snake Malayotyphlops cf. ruficaudus. Our results support convergence among these species in the number of trunk and caudal vertebrae, but not vertebral shape. We also find that the elongate species are relatively slower than their limbed counterparts and move with lower frequency and higher amplitude body undulations, with the exception of Isopachys. This is among the first evidence of locomotor convergence across distantly related, elongate species.

Evolution of fossorial locomotion in the transition from tetrapod to snake-like in lizards.

Dramatic evolutionary transitions in morphology are often assumed to be adaptive in a new habitat. However, these assumptions are rarely tested because such tests require intermediate forms, which are often extinct. In vertebrates, the evolution of an elongate, limbless body is generally hypothesized to facilitate locomotion in fossorial and/or cluttered habitats. However, these hypotheses remain untested because few studies examine the locomotion of species ranging in body form from tetrapod to snake-like. Here, we address these functional hypotheses by testing whether trade-offs exist between locomotion in surface, fossorial and cluttered habitats in Australian Lerista lizards, which include multiple intermediate forms. We found that snake-like species penetrated sand substrates faster than more lizard-like species, representing the first direct support of the adaptation to fossoriality hypothesis. By contrast, body form did not affect surface locomotion or locomotion through cluttered leaf litter. Furthermore, all species with hindlimbs used them during both fossorial and surface locomotion. We found no evidence of a trade-off between fossorial and surface locomotion. This may be either because Lerista employed kinematic strategies that took advantage of both axial- and limb-based propulsion. This may have led to the differential occupation of their habitat, facilitating diversification of intermediate forms.

Angles and waves: intervertebral joint angles and axial kinematics of limbed lizards, limbless lizards, and snakes.

Segmentation gives rise to the anterior-posterior axis in many animals, and in vertebrates this axis comprises serially arranged vertebrae. Modifications to the vertebral column abound, and a recurring, but functionally understudied, change is the elongation of the body through the addition and/or elongation of vertebrae. Here, we compared the vertebral and axial kinematics of the robustly limbed Fire skink (Riopa fernandi) representing the ancestral form, the limbless European glass lizard (Ophisaurus apodus), and the Northern water snake (Nerodia sipedon). We induced these animals to traverse through channels and peg arrays of varied widths and densities, respectively, using high-speed X-ray and light video. We found that even though the snake had substantially more and shorter vertebrae than either lizard, intervertebral joint angles did not differ between species in most treatment levels. All three species decreased the amplitude and wavelength of their undulations as channels narrowed and the lizard species increased wave frequency in narrower channels. In peg arrays, both lizard species decreased wave amplitude, while the snake showed no differences. All three species maintained similar wavelengths and frequencies as peg density increased in most cases. Our results suggest that amplitude is decoupled from wavelength and frequency in all three focal taxa. The combination of musculoskeletal differences and the decoupling of axial kinematic traits likely facilitates the formation of different undulatory waves, thereby allowing limbless species to adopt different modes of locomotion.

The convergent evolution of snake-like forms by divergent evolutionary pathways in squamate reptiles.

Convergent evolution of phenotypes is considered evidence that evolution is deterministic. Establishing if such convergent phenotypes arose through convergent evolutionary pathways is a stronger test of determinism. We studied the evolution of snake-like body shapes in six clades of lizards, each containing species ranging from short-bodied and pentadactyl to long-bodied and limbless. We tested whether body shapes that evolved in each clade were convergent, and whether clades evolved snake-like body shapes following convergent evolutionary pathways. Our analyses showed that indeed species with the same numbers of digits in each clade evolved convergent body shapes. We then compared evolutionary pathways among clades by considering patterns of evolutionary integration and shape of relationship among body parts, patterns of vertebral evolution, and models of digit evolution. We found that all clades elongated their bodies through the addition, not elongation, of vertebrae, and had similar patterns of integration. However, patterns of integration, the body parts that were related by a linear or a threshold model, and patterns of digit evolution differed among clades. These results showed that clades followed different evolutionary pathways. This suggests an important role of historical contingency as opposed to determinism in the convergent evolution of snake-like body shapes.

Are there general laws for digit evolution in squamates? The loss and re-evolution of digits in a clade of fossorial lizards (Brachymeles, Scincinae).

Evolutionary simplification of autopodial structures is a major theme in studies of body-form evolution. Previous studies on amniotes have supported Morse's law, that is, that the first digit reduced is Digit I, followed by Digit V. Furthermore, the question of reversibility for evolutionary digit loss and its implications for "Dollo's law" remains controversial. Here, we provide an analysis of limb and digit evolution for the skink genus Brachymeles. Employing phylogenetic, morphological, osteological, and myological data, we (a) test the hypothesis that digits have re-evolved, (b) describe patterns of morphological evolution, and (c) investigate whether patterns of digit loss are generalizable across taxa. We found strong statistical support for digit, but not limb re-evolution. The feet of pentadactyl species of Brachymeles are very similar to those of outgroup species, while the hands of these lineages are modified (2-3-3-3-2) and a have a reduced set of intrinsic hand muscles. Digit number variation suggests a more labile Digit V than Digit I, contrary to Morse's law. The observed pattern of digit variation is different from that of other scincid lizards (Lerista, Hemiergis, Carlia). Our results present the first evidence of clade-specific modes of digit reduction.

It's just sand between the toes: how particle size and shape variation affect running performance and kinematics in a generalist lizard.

Animals must cope with and be able to move effectively on a variety of substrates. Substrates composed of granular media, such as sand and gravel, are extremely common in nature, and vary tremendously in particle size and shape. Despite many studies of the properties of granular media and comparisons of locomotion between granular and solid substrates, the effects of systematically manipulating these media on locomotion is poorly understood. We studied granular media ranging over four orders of magnitude in particle size, and differing in the amount of particle shape variation, to determine how these factors affected substrate physical properties and sprinting in the generalist lizard Eremias arguta We found that media with intermediate particle sizes had high bulk densities, low angles of stability and low load-bearing capacities. Rock substrates with high shape variation had higher values for all three properties than glass bead substrates with low shape variation. We found that E. arguta had the highest maximum velocities and accelerations on intermediate size particles, and higher velocities on rock than glass beads. Lizards had higher stride frequencies and lower duty factors on intermediate particle size substrates, but their stride lengths did not change with substrate. Our findings suggest that sand and gravel may represent different locomotor challenges for animals. Sand substrates provide animals with an even surface for running, but particles shift underfoot. In contrast, gravel particles are heavy, so move far less underfoot, yet provide the animal with an uneven substrate.

Genetic Bases of Fungal White Rot Wood Decay Predicted by Phylogenomic Analysis of Correlated Gene-Phenotype Evolution.

Fungal decomposition of plant cell walls (PCW) is a complex process that has diverse industrial applications and huge impacts on the carbon cycle. White rot (WR) is a powerful mode of PCW decay in which lignin and carbohydrates are both degraded. Mechanistic studies of decay coupled with comparative genomic analyses have provided clues to the enzymatic components of WR systems and their evolutionary origins, but the complete suite of genes necessary for WR remains undetermined. Here, we use phylogenomic comparative methods, which we validate through simulations, to identify shifts in gene family diversification rates that are correlated with evolution of WR, using data from 62 fungal genomes. We detected 409 gene families that appear to be evolutionarily correlated with WR. The identified gene families encode well-characterized decay enzymes, e.g., fungal class II peroxidases and cellobiohydrolases, and enzymes involved in import and detoxification pathways, as well as 73 gene families that have no functional annotation. About 310 of the 409 identified gene families are present in the genome of the model WR fungus Phanerochaete chrysosporium and 192 of these (62%) have been shown to be upregulated under ligninolytic culture conditions, which corroborates the phylogeny-based functional inferences. These results illuminate the complexity of WR and suggest that its evolution has involved a general elaboration of the decay apparatus, including numerous gene families with as-yet unknown exact functions.

Hindlimb muscle anatomical mechanical advantage differs among joints and stride phases in basilisk lizards.

The vertebrate musculoskeletal system is composed of skeletal levers powered by muscles. Effective mechanical advantage (EMA) and muscle properties influence organismal performance at various tasks. Anatomical mechanical advantage (AMA) is a proxy for EMA that facilitates the study of preserved specimens when many muscles or many species are of interest. AMA is the quotient of in-lever to out-lever length, and quantifies the force-velocity trade-off of a lever, where high AMAs translate into high force, low velocity levers. We studied AMAs, physiological cross-sectional areas (PCSAs), fiber lengths, and fiber widths for 20 hindlimb muscles of the lizard Basiliscus vittatus, moving the hip, knee, and ankle during both the stance and swing phases of the stride. We tested the hypotheses that muscles moving proximal limb joints, and those active during stance, would have characteristics that maximize force. We also tested whether adults had more force-optimized levers than juveniles to compensate for higher body mass. We found no differences between adults and juveniles, but found differences among joints and between stride phases. AMAs were lowest and PCSAs highest for the knee, and PCSA was higher for stance than swing muscles. Fiber width decreased distally, but did not differ between stride phases. Fiber length of stance muscles decreased distally and was highest for swing muscles of the knee. Our findings show that different muscle and lever characteristics allow the knee to be both force- and velocity-optimized, indicating its important role in locomotion.

Tail autotomy, tail size, and locomotor performance in lizards.

The effect of tail autotomy on locomotor performance has been studied in a number of lizard species. Most of these studies (65%) show that tail autotomy has a negative effect on sprint speed, some studies (26%) show no effect of autotomy on sprint speed, and a few (9%) show a positive effect of autotomy on sprint speed. A variety of hypotheses have been proposed to explain the variation across these studies, but none has been tested. We synthesize these data using meta-analysis and then test whether any of four variables explain the variation in how tail autotomy impacts sprint speed: (1) differences in methodology in previous studies, (2) phylogeny, (3) relative tail size, and (4) habitat use. We find little evidence that methodology or habitat use influences how sprint speed changes following tail autotomy. Although the sampling is phylogenetically sparse, phylogeny appears to play a role, with skinks and iguanids showing fairly consistent decreases in speeds after autotomy and with lacertids and geckos showing large variation in how autotomy impacts speed. After removing two outlying species with unusually large and long tails (Takydromus sp.), we find a positive relationship between relative tail size and sprint speed change after autotomy. Lizards with larger tails exhibit a greater change in speed after tail loss. This finding suggests that future studies of tail autotomy and locomotor performance might profitably incorporate variation in tail size and that species-specific responses to autotomy need to be considered.

Vertebral evolution and the diversification of squamate reptiles.

Taxonomic, morphological, and functional diversity are often discordant and independent components of diversity. A fundamental and largely unanswered question in evolutionary biology is why some clades diversify primarily in some of these components and not others. Dramatic variation in trunk vertebral numbers (14 to >300) among squamate reptiles coincides with different body shapes, and snake-like body shapes have evolved numerous times. However, whether increased evolutionary rates or numbers of vertebrae underlie body shape and taxonomic diversification is unknown. Using a supertree of squamates including 1375 species, and corresponding vertebral and body shape data, we show that increased rates of evolution in vertebral numbers have coincided with increased rates and disparity in body shape evolution, but not changes in rates of taxonomic diversification. We also show that the evolution of many vertebrae has not spurred or inhibited body shape or taxonomic diversification, suggesting that increased vertebral number is not a key innovation. Our findings demonstrate that lineage attributes such as the relaxation of constraints on vertebral number can facilitate the evolution of novel body shapes, but that different factors are responsible for body shape and taxonomic diversification.

Alternate pathways of body shape evolution translate into common patterns of locomotor evolution in two clades of lizards.

Body shape has a fundamental impact on organismal function, but it is unknown how functional morphology and locomotor performance and kinematics relate across a diverse array of body shapes. We showed that although patterns of body shape evolution differed considerably between lizards of the Phrynosomatinae and Lerista, patterns of locomotor evolution coincided between clades. Specifically, we found that the phrynosomatines evolved a stocky phenotype through body widening and limb shortening, whereas Lerista evolved elongation through body lengthening and limb shortening. In both clades, relative limb length played a key role in locomotor evolution and kinematic strategies, with long-limbed species moving faster and taking longer strides. In Lerista, the body axis also influenced locomotor evolution. Similar patterns of locomotor evolution were likely due to constraints on how the body can move. However, these common patterns of locomotor evolution between the two clades resulted in different kinematic strategies and levels of performance among species because of their morphological differences. Furthermore, we found no evidence that distinct body shapes are adaptations to different substrates, as locomotor kinematics did not change on loose or solid substrates. Our findings illustrate the importance of studying kinematics to understand the mechanisms of locomotor evolution and phenotype-function relationships.

Directional evolution of stockiness coevolves with ecology and locomotion in lizards.

Although studied in many taxa, directional macroevolution remains difficult to detect and quantify. We present an approach for detecting directional evolution in subclades of species when relatively few species are sampled, and apply it to studying the evolution of stockiness in Phrynosomatine lizards. Our approach is more sensitive to detecting the tempo of directional evolution than other available approaches. We use ancestral reconstruction and phylogenetic mapping of morphology to characterize the direction and magnitude of trait evolution. We demonstrate a directional trend toward stockiness in horned lizards, but not their sister groups, finding that stockier species tend to have relatively short and wide bodies, and relatively short heads, tails, and limbs. Ornstein-Uhlenbeck models show that the directional trend in horned lizards is due to a shift in selective regime and stabilizing selection as opposed to directional selection. Bayesian evolutionary correlation analyses indicate that stockier species run more slowly and eat a larger proportion of ants. Furthermore, species with larger horns tend to be slower and more ant-specialized. Directional evolution toward a stocky body shape has evolved in conjunction with changes in a suite of traits, representing a complex example of directional macroevolution.