A highly conserved ontogenetic limb allometry and its evolutionary significance in the adaptive radiation of Anolis lizards.

Diversifications often proceed along highly conserved, evolutionary trajectories. These patterns of covariation arise in ontogeny, which raises the possibility that adaptive morphologies are biased towards trait covariations that resemble growth trajectories. Here, we test this prediction in the diverse clade of Anolis lizards by investigating the covariation of embryonic growth of 13 fore- and hindlimb bones in 15 species, and compare these to the evolutionary covariation of these limb bones across 267 Anolis species. Our results demonstrate that species differences in relative limb length are established already at hatching, and are resulting from both differential growth and differential sizes of cartilaginous anlagen. Multivariate analysis revealed that Antillean Anolis share a common ontogenetic allometry that is characterized by positive allometric growth of the long bones relative to metapodial and phalangeal bones. This major axis of ontogenetic allometry in limb bones deviated from the major axis of evolutionary allometry of the Antillean Anolis and the two clades of mainland Anolis lizards. These results demonstrate that the remarkable diversification of locomotor specialists in Anolis lizards are accessible through changes that are largely independent from ontogenetic growth trajectories, and therefore likely to be the result of modifications that manifest at the earliest stages of limb development.

Evolution of the locomotor skeleton in Anolis lizards reflects the interplay between ecological opportunity and phylogenetic inertia.

Anolis lizards originated in continental America but have colonized the Greater Antillean islands and recolonized the mainland, resulting in three major groups (Primary and Secondary Mainland and Greater Antillean). The adaptive radiation in the Greater Antilles has famously resulted in the repeated evolution of ecomorphs. Yet, it remains poorly understood to what extent this island radiation differs from diversification on the mainland. Here, we demonstrate that the evolutionary modularity between girdles and limbs is fundamentally different in the Greater Antillean and Primary Mainland Anolis. This is consistent with ecological opportunities on islands driving the adaptive radiation along distinct evolutionary trajectories. However, Greater Antillean Anolis share evolutionary modularity with the group that recolonized the mainland, demonstrating a persistent phylogenetic inertia. A comparison of these two groups support an increased morphological diversity and faster and more variable evolutionary rates on islands. These macroevolutionary trends of the locomotor skeleton in Anolis illustrate that ecological opportunities on islands can have lasting effects on morphological diversification.

Divergent morphological responses to millennia of climate change in two species of bats from Hall's Cave, Texas, USA.

How species will respond to ongoing and future climate change is one of the most important questions facing biodiversity scientists today. The fossil record provides unparalleled insight into past ecological and evolutionary responses to climate change, but the resource remains virtually untapped for many organisms. We use geometric morphometrics and a 25,000 year fossil record to quantify changes in body size and mandible shape through time and across climate regimes for two bat species present in Quaternary paleontological deposits of central Texas: Myotis velifer, a bat distributed throughout the Southwestern US and Mexico that is still found in central Texas today, and Eptesicus fuscus, a bat widely distributed throughout North America that has been extirpated in central Texas. Because of ecogeographic rules like Bergmann's rule, which posits that endotherms are larger in colder environments, we hypothesized that both species were larger during cooler time intervals. Additionally, we hypothesized that both species would show variation in dental morphology across the studied sequence as a response to climate change. While we found a decrease in centroid size-a proxy for --body size-through time for both species, we could not establish a clear relationship between centroid size and temperature alone. However, we did find that specimens from drier environments were significantly larger than those from wetter ones. Furthermore, we found significant dental shape variation between environments reflecting different temperature levels for both species. Yet only M. velifer exhibited significant variation between environments of varying precipitation levels. This result was surprising because present-day populations of E. fuscus are highly variable across both temperature and precipitation gradients. We determined that the morphological change experienced by M. velifer through time, and between warmer and cooler temperatures, was associated with the coronoid process, condylar process, and the mandibular symphysis. These parts play a pivotal role in bite force, so changes in these features might relate to changes in diet. We show that long-term datasets derived from fossil material provide invaluable insight not only into the validity of ecogeographic rules, but also into the adaptive capacities of extant taxa when faced with environmental changes. Our results highlight diverging responses to a variety of climate factors that are relevant to consider in biodiversity research given ongoing global change.

Enhanced locomotor performance on familiar surfaces is uncoupled from morphological plasticity in Anolis lizards.

The radiation of Anolis lizards in the Caribbean is associated with a diversification of the functional match between morphology, habitat use, and locomotor performance. It has been hypothesized that the microhabitat a lizard is reared in can achieve a similar fit of form and function within a species. This predicts that plasticity in the locomotor apparatus is accompanied by changes in perching behavior or improved locomotor performance. To test this, we raised juveniles of two species (Anolis sagrei and Anolis carolinensis) on either broad or narrow surfaces and examined perching behavior and locomotor performance as well as the shape of the pectoral and pelvic girdles, limb length, and thickness of the long bones. Perching behavior was not affected by the habitat surface experienced during ontogeny. However, individuals raised on broad surfaces showed better locomotor performance on broad surfaces, and the magnitude of the effect was as large as the difference between the two species. Both species showed modifications of pectoral and pelvic shape, but only A. carolinensis developed longer limbs on broad surfaces. However, these morphological adjustments induced by physical activity did not explain why lizards raised on broad surfaces performed better. Thus, it appears that early-life experiences can affect both the morphology of the locomotor apparatus and locomotor performance in Anolis lizards, without the two being functionally connected.

Developmental plasticity and evolutionary explanations.

Developmental plasticity looks like a promising bridge between ecological and developmental perspectives on evolution. Yet, there is no consensus on whether plasticity is part of the explanation for adaptive evolution or an optional "add-on" to genes and natural selection. Here, we suggest that these differences in opinion are caused by differences in the simplifying assumptions, and particular idealizations, that enable evolutionary explanation. We outline why idealizations designed to explain evolution through natural selection prevent an understanding of the role of development, and vice versa. We show that representing plasticity as a reaction norm conforms with the idealizations of selective explanations, which can give the false impression that plasticity has no explanatory power for adaptive evolution. Finally, we use examples to illustrate why evolutionary explanations that include developmental plasticity may in fact be more satisfactory than explanations that solely refer to genes and natural selection.

Developmental bias in the fossil record.

The role of developmental bias and plasticity in evolution is a central research interest in evolutionary biology. Studies of these concepts and related processes are usually conducted on extant systems and have seen limited investigation in the fossil record. Here, I identify plasticity-led evolution (PLE) as a form of developmental bias accessible through scrutiny of paleontological material. I summarize the process of PLE and describe it in terms of the environmentally mediated accumulation and release of cryptic genetic variation. Given this structure, I then predict its manifestation in the fossil record, discuss its similarity to quantum evolution and punctuated equilibrium, and argue that these describe macroevolutionary patterns concordant with PLE. Finally, I suggest methods and directions towards providing evidence of PLE in the fossil record and conclude that such endeavors are likely to be highly rewarding.

Ecological innovations in the Cambrian and the origins of the crown group phyla.

Simulation studies of the early origins of the modern phyla in the fossil record, and the rapid diversification that led to them, show that these are inevitable outcomes of rapid and long-lasting radiations. Recent advances in Cambrian stratigraphy have revealed a more precise picture of the early bilaterian radiation taking place during the earliest Terreneuvian Series, although several ambiguities remain. The early period is dominated by various tubes and a moderately diverse trace fossil record, with the classical 'Tommotian' small shelly biota beginning to appear some millions of years after the base of the Cambrian at ca 541 Ma. The body fossil record of the earliest period contains a few representatives of known groups, but most of the record is of uncertain affinity. Early trace fossils can be assigned to ecdysozoans, but deuterostome and even spiralian trace and body fossils are less clearly represented. One way of explaining the relative lack of clear spiralian fossils until about 536 Ma is to assign the various lowest Cambrian tubes to various stem-group lophotrochozoans, with the implication that the groundplan of the lophotrochozoans included a U-shaped gut and a sessile habit. The implication of this view would be that the vagrant lifestyle of annelids, nemerteans and molluscs would be independently derived from such a sessile ancestor, with potentially important implications for the homology of their sensory and nervous systems.