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Figure 2 from: Shaney KJ, Harvey MB, Hamidy A, Kurniawan N, Smith EN (2020) Phylogeny and biogeography of Sumatra´s cloud forest lizards of the genus Dendragama and status of Acanthosaura schneideri. ZooKeys 995: 127-153. https://doi.org/10.3897/zookeys.995.49355
Figure 2 Bayesian tree of Dendragama and other agamid taxa included in our analyses. PD = Pairwise Distance. Mountains associated with Dendragama population sampling are noted. Bronchocela abbreviated as B, Lophocalotes as L, and Pseudocalotes as P.
Figure 1 from: Shaney KJ, Harvey MB, Hamidy A, Kurniawan N, Smith EN (2020) Phylogeny and biogeography of Sumatra´s cloud forest lizards of the genus Dendragama and status of Acanthosaura schneideri. ZooKeys 995: 127-153. https://doi.org/10.3897/zookeys.995.49355
Figure 1 Collection localities of specimens of Dendragama used for comparisons in this study. (T) designates type locality and nearby paralectotype locality (Marapi). White dots represent hypothesized potential locations for new species or divergent populations. Dotted white lines show major biogeographic breaks.
Asymmetric interspecific competition drives shifts in signalling traits in fan-throated lizards
<p>Interspecific competition can occur when species are unable to distinguish between conspecific and heterospecific mates or competitors when they occur in sympatry. Selection in response to interspecific competition can lead to shifts in signalling traits - a process termed as agonistic character displacement. In two fan-throated lizard species- <i>Sitana laticeps</i>and <i>Sarada darwini,</i> females are morphologically indistinguishable and male agonistic signalling behaviour is similar. Consequently, in areas where these species overlap, males engage in interspecific aggressive interactions. To test whether interspecific male aggression between <i>S. laticeps</i> and <i>S. darwini</i> results in agonistic character displacement, we quantified species recognition and signalling behaviour using staged encounter assays with both conspecifics and heterospecifics across sympatric and allopatric populations of both species. We found an asymmetric pattern, wherein males of <i>S. laticeps</i>but not <i>S. darwini</i> showed differences in competitor recognition and agonistic signalling traits (morphology and behaviour) in sympatry compared to allopatry. This asymmetric shift in traits is likely due to differences in competitive abilities between species and can minimize competitive interactions in zones of sympatry. Overall, our results support agonistic character displacement, and highlight the role of asymmetric interspecific competition in driving shifts in social signals. </p>
Data from: Elevation is a stronger predictor of morphological trait divergence than competition in a radiation of tropical lizards
<p><span>1. Adaptations for efficient performance are expected to shape animal morphology based on selection for microhabitat use and ecological forces. The presence of competitor species is predicted to cause niches to contract and enhance trait divergence. Therefore, increased species richness is expected to lead to greater trait divergence, and to result in reduced overlap and similarity between morphologies of sympatric species.</span></p> <p><span>2. We examined patterns of morphospace occupancy and partitioning in the skink fauna of New Guinea, the world's largest tropical island. Because skink species richness is largely decoupled from elevation in New Guinea, we could examine the effects of both factors (as proxies for competition and abiotic conditions), on morphospace occupancy and partitioning.</span></p> <p><span>3. We measured 1860 specimens from 79 species of skinks throughout Papua New Guinea, and examined their morphospace occupancy in a spatial context. We calculated for each assemblage within equal-area cells, the volume of morphospace occupied by all skinks, the mean volume occupied per species, and the mean distance and overlap between all species pairs. We then examined if these metrics are related to species richness and elevation.</span></p> <p><span>4. Elevation is a stronger predictor of morphospace occupancy than species richness. As elevation increases intraspecific variation decreases and morphologies become more similar to each other, such that overall morphospace occupancy decreases. Highland skinks are, on average, smaller, thinner, and shorter limbed than lowland species.</span></p> <p><span>5. We hypothesize that harsh climates in the New Guinea highland habitats impose strong selection on skinks to occupy specific areas of morphospace that facilitate efficient thermoregulation in sub-optimal thermal conditions. We conclude that the effect of competition on trait divergence on a community and assemblage scale is eclipsed by abiotic selection pressures in these harsh environments.</span></p>
Data from: Thermal niche evolution across replicated Anolis lizard adaptive radiations
Elucidating how ecological and evolutionary mechanisms interact to produce and maintain biodiversity is a fundamental problem in evolutionary ecology. We investigate this issue by focusing on how physiological evolution affects performance and species coexistence along the thermal niche axis in replicated radiations of Anolis lizards, groups best known for resource partitioning based on morphological divergence. We find repeated divergence in thermal physiology within these radiations, and that this divergence significantly affects performance within natural thermal environments. Morphologically similar species that co-occur invariably differ in their thermal physiology, providing evidence that physiological divergence facilitates species co-existence within anole communities. Despite repeated divergence in traits of demonstrable ecological importance, phylogenetic comparative analyses indicate that physiological traits have evolved more slowly than key morphological traits related to the structural niche. Phylogenetic analyses also reveal that physiological divergence is correlated with divergence in broad-scale habitat climatic features commonly used to estimate thermal niche evolution, but that the latter incompletely predicts variation in the former. We provide comprehensive evidence for repeated adaptive evolution of physiological divergence within Anolis adaptive radiations, including the complementary roles of physiological and morphological divergence in promoting community-level diversity. We recommend greater integration of performance-based traits into analyses of climatic niche evolution, as they facilitate a more complete understanding of the phenotypic and ecological consequences of climatic divergence.
Data from: The role of bite force in the evolution of head shape and head shape dimorphism in Anolis lizards
1. Patterns of convergent evolution in head shape, combined with performance measures, provide ideal opportunities to understand the processes driving its evolution. Anole lizards represent an excellent subject to test this, as recurrent habitat specialists or ecomorphs evolved independently across different islands. 2. We show that phenotypic similarity corresponds to both phylogenetic similarity and similarity in habitat, indicating that there is convergent evolution in head shape among ecomorphs. Moreover, we show that the evolution of tall, wide heads correlates with the evolution of higher bite forces, driving head shape variation among and within ecomorphs. 3. In addition, the processes affecting head shape variation can differ between sexes, leading to sexual head shape dimorphism. These processes might, however, still depend on the habitat. Consequently, there could also be convergent evolution in head shape dimorphism among ecomorphs. 4. We found no evidence for convergent evolution in sexual head shape dimorphism. Moreover, the sexual head shape dimorphism correlates poorly with bite force, suggesting that intersexual head shape differences are related to other functions. Different processes are thus driving the evolution of head shape and head shape dimorphism.
Data from: Sexual dimorphism explains residual variance around the survival-reproduction tradeoff in lizards: implications for sexual conflict over life-history evolution
The tradeoff between survival and reproduction is a central feature of life-history variation, but few studies have sought to explain why females of some species exhibit relatively lower survival than expected for a given level of reproductive effort. Intralocus sexual conflict theory proposes that sex differences in selection on survival and reproductive effort may, by virtue of shared genes underlying these components of fitness, prevent females from optimizing this life-history tradeoff. To test this hypothesis, we used a phylogenetically based comparative analysis of published estimates for mean annual survival and reproductive effort from females of 82 lizard species to (1) characterize the tradeoff between survival and reproduction, and (2) test whether variation around this tradeoff is explained by sexual size dimorphism (SSD), a potential proxy for sexual conflict over life-history traits. Across species, we found a strong negative correlation between mean annual survival and reproductive effort, confirming this classic life-history tradeoff. Although residual variance around this tradeoff is unrelated to the absolute magnitude of SSD, it is strongly related to the direction of SSD. Specifically, we found that females have lower survival than expected for a given level of reproductive effort in female-larger species, whereas they have higher survival than expected in male-larger species. Given that female-larger SSD is thought to reflect selection for increased fecundity, our results suggest that intralocus sexual conflict may be particularly likely to constrain female life-history evolution in situations where increased reproductive effort is favored, but the phenotypes that facilitate this increase (e.g., body size) are constrained by antagonistic selection on males.
Data from: How should genes and taxa be sampled for phylogenomic analyses with missing data? An empirical study in iguanian lizards
Targeted sequence capture is becoming a widespread tool for generating large phylogenomic data sets to address difficult phylogenetic problems. However, this methodology often generates data sets in which increasing the number of taxa and loci increases amounts of missing data. Thus, a fundamental (but still unresolved) question is whether sampling should be designed to maximize sampling of taxa or genes, or to minimize the inclusion of missing data cells. Here, we explore this question for an ancient, rapid radiation of lizards, the pleurodont iguanians. Pleurodonts include many well-known clades (e.g., anoles, basilisks, iguanas, and spiny lizards) but relationships among families have proven difficult to resolve strongly and consistently using traditional sequencing approaches. We generated up to 4921 ultraconserved elements with sampling strategies including 16, 29, and 44 taxa, from 1179 to approximately 2.4 million characters per matrix and approximately 30% to 60% total missing data. We then compared mean branch support for interfamilial relationships under these 15 different sampling strategies for both concatenated (maximum likelihood) and species tree (NJst) approaches (after showing that mean branch support appears to be related to accuracy). We found that both approaches had the highest support when including loci with up to 50% missing taxa (matrices with ∼40–55% missing data overall). Thus, our results show that simply excluding all missing data may be highly problematic as the primary guiding principle for the inclusion or exclusion of taxa and genes. The optimal strategy was somewhat different for each approach, a pattern that has not been shown previously. For concatenated analyses, branch support was maximized when including many taxa (44) but fewer characters (1.1 million). For species-tree analyses, branch support was maximized with minimal taxon sampling (16) but many loci (4789 of 4921). We also show that the choice of these sampling strategies can be critically important for phylogenomic analyses, since some strategies lead to demonstrably incorrect inferences (using the same method) that have strong statistical support. Our preferred estimate provides strong support for most interfamilial relationships in this important but phylogenetically challenging group.
Data from: Developmental dynamics of ecomorphological convergence in a transcontinental lizard radiation
Phenotypic convergence has confounded evolutionary biologists for centuries, explained as adaptations to shared selective pressures, or alternatively, the result of limited developmental pathways. We tested the relative roles of adaptation and constraint in generating convergent cranial morphologies across a large lizard radiation, the Lacertidae, whose members inhabit diverse environments throughout the Old World and display high amounts of homoplasy associated with ecological niche. Using three-dimensional X-ray computed tomography, we quantified cranial shape variation associated with ontogeny, allometry, and ecology, covering all lacertid genera and one-third of species diversity. Landmark-based geometric morphometrics showed that cranial shape varied significantly among biomes, with substantial convergence among arid-dwelling lineages. Comparisons of species ontogenetic growth trajectories between biomes revealed that allometric postdisplacement, as evidenced by decreased elevation of a constant slope, drives the convergent paedomorphic appearance of independent arid-dwelling forms. We hypothesize that observed heterochronic changes reflect temporal compression of ancestral life history in response to extreme environments, with associated phenotypes occurring as by-products of adaptive shifts in reproductive investment. Although allometry has long been considered a developmental constraint, our results demonstrate that allometric flexibility during early ontogeny produces convergent ecomorphologies over vast temporal and spatial scales, thus dramatically obscuring underlying phylogenetic signals.
Data from: Sex-specific density-dependent secretion of glucocorticoids in lizards: insights from laboratory and field experiments
Negative density feedbacks have been extensively described in animal species and involve both consumptive (i.e. trophic interactions) and non-consumptive (i.e. social interactions) mechanisms. Glucocorticoids are a major component of the physiological stress response and homeostasis, and therefore make a good candidate for proximate determinants of negative density feedbacks. Here, we combined laboratory and field experiments with enclosed populations to investigate the relationship between density, social stress and plasma corticosterone levels in the common lizard Zootoca vivipara. This species exhibits strong negative density feedbacks that affect females more than males, and its life history is sensitive to experimentally-induced chronic elevation of corticosterone plasma levels. We found that prolonged crowding in the laboratory can trigger a chronic secretion of corticosterone independent from food restriction. In the field experiments, corticosterone levels of females were not affected by population density. Corticosterone levels of males increased with population density but only during the late activity season in a first field experiment where we manipulated density. They also increased with density during the mating season but only in populations with a female-biased sex ratio in a second field experiment where we crossed manipulated density and adult sex ratio. Altogether, our results provide limited evidence for a role of basal corticosterone secretion in density feedbacks in this species. Context and density-dependent effects in males may arise from changes in behavior caused by competition for resources, male–male competition, and mating.
Data from: On dangerous ground: the evolution of body armour in cordyline lizards
Animal body armour is often considered an adaptation that protects prey against predatory attacks, yet comparative studies that link the diversification of these allegedly protective coverings to differential predation risk or pressure are scarce. Here, we examine the evolution of body armour, including spines and osteoderms, in Cordylinae, a radiation of southern African lizards. Using phylogenetic comparative methods, we attempt to identify the ecological and environmental correlates of body armour that may hint at the selective pressures responsible for defensive trait diversification. Our results show that species inhabiting arid environments are more likely to possess elaborated body armour, specifically osteoderms. We did not find any effect of estimated predation pressure or risk on the degree of body armour. These findings suggest that body armour might not necessarily evolve in response to direct interactions with predators, but rather as a result of increased habitat-mediated predation risk. Furthermore, we discuss the possibility that osteoderms might have been shaped by factors unrelated to predation.
Data from: Little to fear: largest lizard predator induces weak defense responses in ungulate prey
Non-consumptive effects can strongly influence apex predator ecological function. These effects arise because prey produce often induce costly phenotypic responses to mitigate predation risk. Yet because predator-prey interactions are complex, prey defences may vary considerably. We investigated if the Komodo dragon (Varanus komodoensis), an reptile apex predator, induced multi-scale anti-predator responses in key prey, the Rusa deer (Cervus timorensis) and the wild pig (Sus scrofa). To this end, we examined the temporal and spatial partitioning of habitats by predator and prey, determined the size of ungulate groups as a function of risk, and assessed changes in individual behavior of prey individuals exposed to predator kairomones at feeding stations. Komodo dragon, deer and pig populations exhibited significant, but subtle differences in three habitat preferences, that otherwise indicated high niche overlap. Komodo dragon predation risk, alongside other commonly considered predictor variables did not affect deer or pig group size. With the exception of one individual-based vigilance type behavior in pigs, no other anti-predator behavior, including reduced food consumption, significantly varied in the presence of predator odour cue at feeding stations. Overall our results indicated limited evidence for anti-predator behavior and suggest Komodo dragons exert weak non-consumptive effects of predation in ungulates. However, weak predatory interactions could be beneficial in island ecosystems as it could promote predator-prey co-existence that reduces extinction risk.
Data from: How phylogeny and foraging ecology drive the level of chemosensory exploration in lizards and snakes
The chemical senses are crucial for squamates (lizards and snakes). The extent to which squamates utilize their chemosensory system, however, varies greatly among taxa and species' foraging strategies, and played an influential role in squamate evolution. In lizards, Scleroglossa evolved a state where species use chemical cues to search for food (active-foragers), while Iguania retained the use of vision to hunt prey (ambush-foragers). However, such strict dichotomy is flawed since shifts in foraging modes have occurred in all clades. Here, we attempted to disentangle effects of foraging ecology from phylogenetic trait conservatism as leading cause of the disparity in chemosensory investment among squamates. To do so, we used species' tongue-flick rate (TFR) in absence of ecological relevant chemical stimuli as a proxy for its fundamental level of chemosensory investigation, i.e. baseline TFR. Based on literature data of nearly 100 species and using phylogenetic comparative methods, we tested whether and how foraging mode and diet affect baseline TFR. Our results show that baseline TFR is higher in active than ambush foragers. Although baseline TFRs appear phylogenetically stable in some lizard taxa, that is a consequence of concordant stability of foraging mode: when foraging mode shifts within taxa, so does baseline TFR. Also, baseline TFR is a good predictor of prey chemical discriminatory ability, as we established a strong positive relationship between baseline TFR and TFR in response to prey. Baseline TFR is unrelated to diet. Essentially, foraging mode, not phylogenetic relatedness, drives convergent evolution of similar levels of squamate chemosensory investigation.
Data from: Novel approaches for phylogenetic inference from morphological data and total-evidence dating in squamate reptiles (lizards, snakes, and amphisbaenians)
Here, I combine previously underutilized models and priors to perform more biologically-realistic phylogenetic inference from morphological data, with an example from squamate reptiles. When coding morphological characters, it is often possible to denote ordered states with explicit reference to observed or hypothetical ancestral conditions. Using this logic, we can integrate across character-state labels and estimate meaningful rates of forward and backwards transitions from plesiomorphy to apomorphy. I refer to this approach as MkA, for 'asymmetric.' The MkA model incorporates the biological reality of limited reversal for many phylogenetically informative characters, and significantly increases likelihoods in the empirical datasets. Despite this, the phylogeny of Squamata remains contentious. Total-evidence analyses using combined morphological and molecular data and the MkA approach tend towards recent consensus estimates supporting a nested Iguania. However, support for this topology is not unambiguous across datasets or analyses, and no mechanism has been proposed to explain the widespread incongruence between partitions, or the hidden support for various topologies in those partitions. Furthermore, different morphological datasets produced by different authors contain both different characters and different states for the same or similar characters, resulting in drastically different placements for many important fossil lineages. Effort is needed to standardize ontology for morphology, resolve incongruence, and estimate a robust phylogeny. The MkA approach provides a preliminary avenue for investigating morphological evolution while accounting for temporal evidence and asymmetry in character-state changes.
Data from: Experimental contact zones reveal causes and targets of sexual selection in hybridizing lizards
Divergence in sexually selected traits in allopatry should affect the degree and direction of hybridization. However, few studies have established the causes and targets of sexual selection during secondary contact. Common wall lizards (Podarcis muralis) from north-central Italy have highly exaggerated male sexual traits compared to populations in Western Europe. Using experimental populations, we show that this creates asymmetries in male dominance, spatial habitat use and reproductive success upon secondary contact. Hybridization occurred almost exclusively between males of the Italian lineage and females of the Western European lineage. We provide evidence to suggest stronger ongoing selection on male sexual traits within the dominant Italian lineage. However, these same characters did not predict hybridization, and hybrid matings contributed little to variance in male reproductive success. Instead, most hybrid offspring were sired by Italian males displaying phenotypes associated with lower within-lineage reproductive success. Thus, highly directional hybridization arises because some Italian males are out-competed within their own lineage but remain competitive relative to males of the other lineage. This pattern of hybridization is consistent with the direction of introgression in natural contact zones, but our data suggest that sexual selection acting through hybridization may be weak at the leading edge of natural hybrid zones.
Data from: The evolution of colour pattern complexity: selection for conspicuousness favours contrasting within-body colour combinations in lizards
Many animals display complex colour patterns that comprise several adjacent, often contrasting colour patches. Combining patches of complementary colours increases the overall conspicuousness of the complex pattern, enhancing signal detection. Therefore, selection for conspicuousness may act not only on the design of single colour patches, but also on their combination. Contrasting long- and short-wavelength colour patches are located on the ventral and lateral surfaces of many lacertid lizards. As the combination of long- and short-wavelength-based colours generates local chromatic contrast, we hypothesized that selection may favour the co-occurrence of lateral and ventral contrasting patches, resulting in complex colour patterns that maximize the overall conspicuousness of the signal. To test this hypothesis, we performed a comparative phylogenetic study using a categorical colour classification based on spectral data and descriptive information on lacertid coloration collected from the literature. Our results demonstrate that conspicuous ventral (long-wavelength-based) and lateral (short-wavelength-based) colour patches co-occur throughout the lacertid phylogeny more often than expected by chance, especially in the subfamily Lacertini. These results suggest that selection promotes the evolution of the complex pattern rather than the acquisition of a single conspicuous colour patch, possibly due to the increased conspicuousness caused by the combination of colours with contrasting spectral properties.
Data from: Does adaptive radiation of a host lineage promote ecological diversity of its bacterial communities? A test using gut microbiota of Anolis lizards
Adaptive radiations provide unique opportunities to test whether and how recent ecological and evolutionary diversification of host species structures the composition of entire bacterial communities. We used 16S rRNA gene sequencing of faecal samples to test for differences in the gut microbiota of six species of Puerto Rican Anolis lizards characterized by the evolution of distinct 'ecomorphs' related to differences in habitat use. We found substantial variation in the composition of the microbiota within each species and ecomorph (trunk-crown, trunk-ground, grass-bush), but no differences in bacterial alpha diversity among species or ecomorphs. Beta diversity analyses revealed subtle but significant differences in bacterial composition related to host phylogeny and species, but these differences were not consistently associated with Anolis ecomorph. Comparison of a trunk-ground species from this clade (A. cristatellus) with a distantly related member of the same ecomorph class (A. sagrei) where the two species have been introduced and are now sympatric in Florida revealed pronounced differences in the alpha diversity and beta diversity of their microbiota despite their ecological similarity. Comparisons of these populations with allopatric conspecifics also revealed geographic differences in bacterial alpha diversity and beta diversity within each species. Finally, we observed high intraindividual variation over time and strong effects of a simplified laboratory diet on the microbiota of A. sagrei. Collectively, our results indicate that bacterial communities are only weakly shaped by the diversification of their lizard hosts due to the strikingly high levels of bacterial diversity and variation observed within Anolis species.
Data from: Habitat- and season-specific temperatures affect phenotypic development of hatchling lizards
Embryonic environments influence phenotypic development, but relatively few experiments have explored the effects of natural environmental variation. We incubated eggs of the lizard Anolis sagrei under conditions that mimicked natural spatial and temporal thermal variation to determine their effects on offspring morphology and performance. Incubation temperatures mimicked two microhabitats (open, shade) at two different times of the incubation season (April, July). Egg survival, incubation duration and offspring size were influenced by interactions between habitat- and season-specific nest temperatures, and locomotor performance was influenced primarily by temporal factors. These findings highlight the importance of spatial and temporal environmental variation in generating variation in fitness-related phenotypes.
Data from: Comparative evolution of an archetypal adaptive radiation: innovation and opportunity in Anolis lizards
Adaptive radiation is a widely recognized pattern of evolution wherein substantial phenotypic change accompanies rapid speciation. Adaptive radiation may be triggered by environmental opportunities resulting from dispersal to new areas or via the evolution of traits, called key innovations, that allow invasion of new niches. Species sampling is a known source of bias in many comparative analyses, yet classic adaptive radiations have not been studied comparatively with comprehensively sampled phylogenies. In this study we use unprecedented comprehensive phylogenetic sampling of Anolis lizard species to examine comparative evolution in this well-studied adaptive radiation. We compare adaptive radiation models within Anolis and in the Anolis clade and a potential sister lineage, the Corytophanidae. We find evidence for island (i.e., opportunity) effects and no evidence for trait (i.e., key innovation) effects causing accelerated phenotypic evolution within Anolis. However, island effects are scale dependent: when Anolis and Corytophanidae are analyzed together, no island effect is evident. We find no evidence for an island effect on speciation rate, and tenuous evidence for greater speciation rate due to trait effects. These results suggest the need for precision in treatments of classic adaptive radiations such as Anolis, and further refinement of the concept of adaptive radiation.
Data from: The evolution of bipedal running in lizards suggests a consequential origin may be exploited in later lineages.
The origin of bipedal locomotion in lizards is unclear. Modeling studies have suggested that bipedalism may be an exaptation, a byproduct of features originally designed to increase maneuverability, which were only later exploited. Measurement of the body center of mass (BCOM) in 124 species of lizards confirms a significant rearward shift among bipedal lineages. Further racetrack trials showed a significant acceleration threshold between bipedal and quadrupedal runs. These suggest good general support for a passive bipedal model, in which the combination of these features lead to passive lifting of the front of the body. However, variation in morphology could only account for 56% of the variation in acceleration thresholds, suggesting that dynamics have a significant influence on bipedalism. Deviation from the passive bipedal model was compared with node age, supporting an increase in the influence of dynamics over time. Together, these results show that bipedalism may have first arisen as a consequence of acceleration and a rearward shift in the BCOM, but subsequent linages have exploited this consequence to become bipedal more often, suggesting that bipedalism in lizards may convey some advantage. Exploitation of bipedalism was also associated with increased rates of phenotypic diversity, suggesting exploiting bipedalism may promote adaptive radiation.
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