Journal Articles: 2011 - 2010

Journal Article
A. Herrel, M. DaCosta Cottam, K. Godbeer, T. Sanger, and J. B. Losos. 2011. “An ecomorphological analysis of native and introduced populations of the endemic lizard Anolis maynardi of the Cayman Islands.” Breviora, 522: 1-10.
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A. C. Algar and J. B. Losos. 2011. “Evolutionary assembly of island faunas reverses the classic island-mainland richness difference in Anolis lizards.” Journal of Biogeography, 38: 1125-1137.
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J. Alfoldi, F. Di Palma, M. Grabherr, C. Williams, L. Kong, E. Mauceli, P. Russell, C. B. Lowe, R.E. Glor, J. D. Jaffe, D. A. Ray, S. Boissinot, AM Shedlock, C. Botka, T. A. Castoe, J. K. Colbourne, M. K. Fujita, R. G. Moreno, B. F. ten Hallers, D. Haussler, A. Heger, D. Heiman, D. E. Janes, J. Johnson, P. J. de Jong, M. Y. Koriabine, M. Lara, P. A. Novick, C. L. Organ, S. E. Peach, S. Poe, D.D. Pollock, K. de Queiroz, T. Sanger, S. Searle, J. D. Smith, Z. Smith, R. Swofford, J. Turner-Maier, J. Wade, S. Young, A. Zadissa, SV Edwards, T. C. Glenn, C. J. Schneider, J. B. Losos, E. S. Lander, M. Breen, C. P. Ponting, and K. Lindblad-Toh. 2011. “The genome of the green anole lizard and a comparative analysis with birds and mammals.” Nature, 477: 587-91. Abstract

The evolution of the amniotic egg was one of the great evolutionary innovations in the history of life, freeing vertebrates from an obligatory connection to water and thus permitting the conquest of terrestrial environments. Among amniotes, genome sequences are available for mammals and birds, but not for non-avian reptiles. Here we report the genome sequence of the North American green anole lizard, Anolis carolinensis. We find that A. carolinensis microchromosomes are highly syntenic with chicken microchromosomes, yet do not exhibit the high GC and low repeat content that are characteristic of avian microchromosomes. Also, A. carolinensis mobile elements are very young and diverse-more so than in any other sequenced amniote genome. The GC content of this lizard genome is also unusual in its homogeneity, unlike the regionally variable GC content found in mammals and birds. We describe and assign sequence to the previously unknown A. carolinensis X chromosome. Comparative gene analysis shows that amniote egg proteins have evolved significantly more rapidly than other proteins. An anole phylogeny resolves basal branches to illuminate the history of their repeated adaptive radiations.

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D. C. Collar, 2nd Schulte, J. A., and J. B. Losos. 2011. “Evolution of extreme body size disparity in monitor lizards (Varanus).” Evolution, 65: 2664-80. Abstract

Many features of species' biology, including life history, physiology, morphology, and ecology are tightly linked to body size. Investigation into the causes of size divergence is therefore critical to understanding the factors shaping phenotypic diversity within clades. In this study, we examined size evolution in monitor lizards (Varanus), a clade that includes the largest extant lizard species, the Komodo dragon (V. komodoensis), as well as diminutive species that are nearly four orders of magnitude smaller in adult body mass. We demonstrate that the remarkable body size disparity of this clade is a consequence of different selective demands imposed by three major habitat use patterns-arboreality, terrestriality, and rock-dwelling. We reconstructed phylogenetic relationships and ancestral habitat use and applied model selection to determine that the best-fitting evolutionary models for species' adult size are those that infer oppositely directed adaptive evolution associated with terrestriality and rock-dwelling, with terrestrial lineages evolving extremely large size and rock-dwellers becoming very small. We also show that habitat use affects the evolution of several ecologically important morphological traits independently of body size divergence. These results suggest that habitat use exerts a strong, multidimensional influence on the evolution of morphological size and shape disparity in monitor lizards.

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The past 30 years have seen a revolution in comparative biology. Before that time, systematics was not at the forefront of the biological sciences, and few scientists considered phylogenetic relationships when investigating evolutionary questions. By contrast, systematic biology is now one of the most vigorous disciplines in biology, and the use of phylogenies not only is requisite in macroevolutionary studies but also has been applied to a wide range of topics and fields that no one could possibly have envisioned 30 years ago. My message is simple: phylogenies are fundamental to comparative biology, but they are not the be-all and end-all. Phylogenies are powerful tools for understanding the past, but like any tool, they have their limitations. In addition, phylogenies are much more informative about pattern than they are about process. The best way to fully understand the past-both pattern and process-is to integrate phylogenies with other types of historical data as well as with direct studies of evolutionary process.

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J. B. Losos and R. M. Pringle. 2011. “Competition, predation and natural selection in island lizards.” Nature, 475: E1-2; discussion E3.
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J. B. Losos. 2011. “Convergence, adaptation, and constraint.” Evolution, 65: 1827-40. Abstract

Convergent evolution of similar phenotypic features in similar environmental contexts has long been taken as evidence of adaptation. Nonetheless, recent conceptual and empirical developments in many fields have led to a proliferation of ideas about the relationship between convergence and adaptation. Despite criticism from some systematically minded biologists, I reaffirm that convergence in taxa occupying similar selective environments often is the result of natural selection. However, convergent evolution of a trait in a particular environment can occur for reasons other than selection on that trait in that environment, and species can respond to similar selective pressures by evolving nonconvergent adaptations. For these reasons, studies of convergence should be coupled with other methods-such as direct measurements of selection or investigations of the functional correlates of trait evolution-to test hypotheses of adaptation. The independent acquisition of similar phenotypes by the same genetic or developmental pathway has been suggested as evidence of constraints on adaptation, a view widely repeated as genomic studies have documented phenotypic convergence resulting from change in the same genes, sometimes even by the same mutation. Contrary to some claims, convergence by changes in the same genes is not necessarily evidence of constraint, but rather suggests hypotheses that can test the relative roles of constraint and selection in directing phenotypic evolution.

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J.J. Kolbe, L. J. Revell, B. Szekely, 3rd Brodie, E. D., and J. B. Losos. 2011. “Convergent evolution of phenotypic integration and its alignment with morphological diversification in Caribbean Anolis ecomorphs.” Evolution, 65: 3608-24. Abstract

The adaptive landscape and the G-matrix are keys concepts for understanding how quantitative characters evolve during adaptive radiation. In particular, whether the adaptive landscape can drive convergence of phenotypic integration (i.e., the pattern of phenotypic variation and covariation summarized in the P-matrix) is not well studied. We estimated and compared P for 19 morphological traits in eight species of Caribbean Anolis lizards, finding that similarity in P among species was not correlated with phylogenetic distance. However, greater similarity in P among ecologically similar Anolis species (i.e., the trunk-ground ecomorph) suggests the role of convergent natural selection. Despite this convergence and relatively deep phylogenetic divergence, a large portion of eigenstructure of P is retained among our eight focal species. We also analyzed P as an approximation of G to test for correspondence with the pattern of phenotypic divergence in 21 Caribbean Anolis species. These patterns of covariation were coincident, suggesting that either genetic constraint has influenced the pattern of among-species divergence or, alternatively, that the adaptive landscape has influenced both G and the pattern of phenotypic divergence among species. We provide evidence for convergent evolution of phenotypic integration for one class of Anolis ecomorph, revealing yet another important dimension of evolutionary convergence in this group.

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R. Boistel, A. Herrel, R. Lebrun, G. Daghfous, P. Tafforeau, J. B. Losos, and B. Vanhooydonck. 2011. “Shake rattle and roll: the bony labyrinth and aerial descent in squamates.” Integr. Comp. Biol. , 51: 957-68. Abstract

Controlled aerial descent has evolved many times independently in vertebrates. Squamates (lizards and snakes) are unusual in that respect due to the large number of independent origins of the evolution of this behavior. Although some squamates such as flying geckos of the genus Ptychozoon and the flying dragons of the genus Draco show obvious adaptations including skin flaps or enlarged ribs allowing them to increase their surface area and slow down their descent, many others appear unspecialized. Yet, specializations can be expected at the level of the sensory and neural systems allowing animals to maintain stability during controlled aerial descent. The vestibular system is a likely candidate given that it is an acceleration detector and is well-suited to detect changes in pitch, roll and yaw. Here we use conventional and synchrotron muCT scans to quantify the morphology of the vestibular system in squamates able to perform controlled aerial descent compared to species characterized by a terrestrial or climbing life style. Our results show the presence of a strong phylogenetic signal in the data with the vestibular system in species from the same family being morphologically similar. However, both our shape analysis and an analysis of the dimensions of the vestibular system showed clear differences among animals with different life-styles. Species able to perform a controlled aerial descent differed in the position and shape of the inner ear, especially of the posterior ampulla. Given the limited stability of squamates against roll and the fact that the posterior ampulla is tuned to changes in roll this suggests an adaptive evolution of the vestibular system in squamates using controlled aerial descent. Future studies testing for similar differences in other groups of vertebrates known to use controlled aerial descent are needed to test the generality of this observation.

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K. Kusumi, R. J. Kulathinal, A. Abzhanov, S. Boissinot, N. G. Crawford, B. C. Faircloth, T. C. Glenn, D. E. Janes, J. B. Losos, D. B. Menke, S. Poe, T. J. Sanger, C. J. Schneider, J. Stapley, J. Wade, and J. Wilson-Rawls. 2011. “Developing a community-based genetic nomenclature for anole lizards.” BMC Genomics, 12: 554. Abstract

BACKGROUND: Comparative studies of amniotes have been hindered by a dearth of reptilian molecular sequences. With the genomic assembly of the green anole, Anolis carolinensis available, non-avian reptilian genes can now be compared to mammalian, avian, and amphibian homologs. Furthermore, with more than 350 extant species in the genus Anolis, anoles are an unparalleled example of tetrapod genetic diversity and divergence. As an important ecological, genetic and now genomic reference, it is imperative to develop a standardized Anolis gene nomenclature alongside associated vocabularies and other useful metrics. RESULTS: Here we report the formation of the Anolis Gene Nomenclature Committee (AGNC) and propose a standardized evolutionary characterization code that will help researchers to define gene orthology and paralogy with tetrapod homologs, provide a system for naming novel genes in Anolis and other reptiles, furnish abbreviations to facilitate comparative studies among the Anolis species and related iguanid squamates, and classify the geographical origins of Anolis subpopulations. CONCLUSIONS: This report has been generated in close consultation with members of the Anolis and genomic research communities, and using public database resources including NCBI and Ensembl. Updates will continue to be regularly posted to new research community websites such as lizardbase. We anticipate that this standardized gene nomenclature will facilitate the accessibility of reptilian sequences for comparative studies among tetrapods and will further serve as a template for other communities in their sequencing and annotation initiatives.

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T.J. Hagey, J. B. Losos, and L. J. Harmon. 2010. “Cruise foraging of invasive chameleons (Chamaeleo jacksonii xantholophus) in Hawai'i.” Breviora, 519.
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L. Rodríguez Schettino, J. B. Losos, P. E. Hertz, K. de Quieroz, A.R. Chamizo, M. Leal, and V. Rivalta González. 2010. “The anoles of Soroa: Aspects of their ecological relationships.” Breviora, 520: 1-22.
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D.L. Mahler, L. J. Revell, R.E. Glor, and J. B. Losos. 2010. “Ecological opportunity and the rate of morphological evolution in the diversification of Greater Antillean anoles.” Evolution, 64: 2731-45. Abstract

The pace of phenotypic diversification during adaptive radiation should decrease as ecological opportunity declines. We test this prediction using phylogenetic comparative analyses of a wide range of morphological traits in Greater Antillean Anolis lizards. We find that the rate of diversification along two important axes of Anolis radiation-body size and limb dimensions-decreased as opportunity declined, with opportunity quantified either as time elapsed in the radiation or as the diversity of competing anole lineages inferred to have been present on an island at different times in the past. Most previous studies of the ecological opportunity hypothesis have focused on the rate of species diversification; our results provide a complementary perspective, indicating that the rate of phenotypic diversification declines with decreasing opportunity in an adaptive radiation.

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T. J. Ord, J. A. Stamps, and J. B. Losos. 2010. “Adaptation and plasticity of animal communication in fluctuating environments.” Evolution, 64: 3134-48. Abstract

Adaptations that facilitate the reception of long-range signals under challenging conditions are expected to generate signal diversity when species communicate in different habitats. Although we have a general understanding of how individual communicating animals cope with conditions influencing signal detection, the extent to which plasticity and evolutionary changes in signal characteristics contribute to interspecific differences in signaling behavior is unclear. We quantified the visual displays of free-living lizards and environmental variables known to influence display detection for multiple species from two separate island radiations. We found evidence of both adaptive evolution and adaptive plasticity in display characteristics as a function of environmental conditions, but plasticity accounted for most of the observed differences in display behavior across species. At the same time, prominent differences between the two island radiations existed in aspects of signaling behavior, unrelated to the environment. Past evolutionary events have therefore played an important role in shaping the way lizards adjust their signals to challenges in present-day environments. In addition to showing how plasticity contributes to interspecific differences in communication signals, our findings suggest the vagaries of evolution can in itself lead to signal variation between species.

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D. C. Collar, 2nd Schulte, J. A., B. C. O'Meara, and J. B. Losos. 2010. “Habitat use affects morphological diversification in dragon lizards.” Journal of Evolutionary Biology, 23: 1033-49. Abstract

Habitat use may lead to variation in diversity among evolutionary lineages because habitats differ in the variety of ways they allow for species to make a living. Here, we show that structural habitats contribute to differential diversification of limb and body form in dragon lizards (Agamidae). Based on phylogenetic analysis and ancestral state reconstructions for 90 species, we find that multiple lineages have independently adopted each of four habitat use types: rock-dwelling, terrestriality, semi-arboreality and arboreality. Given these reconstructions, we fit models of evolution to species' morphological trait values and find that rock-dwelling and arboreality limit diversification relative to terrestriality and semi-arboreality. Models preferred by Akaike information criterion infer slower rates of size and shape evolution in lineages inferred to occupy rocks and trees, and model-averaged rate estimates are slowest for these habitat types. These results suggest that ground-dwelling facilitates ecomorphological differentiation and that use of trees or rocks impedes diversification.

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Adaptive radiation refers to diversification from an ancestral species that produces descendants adapted to use a great variety of distinct ecological niches. In this review, I examine two aspects of adaptive radiation: first, that it results from ecological opportunity and, second, that it is deterministic in terms of its outcome and evolutionary trajectory. Ecological opportunity is usually a prerequisite for adaptive radiation, although in some cases, radiation can occur in the absence of preexisting opportunity. Nonetheless, many clades fail to radiate although seemingly in the presence of ecological opportunity; until methods are developed to identify and quantify ecological opportunity, the concept will have little predictive utility in understanding a priori when a clade might be expected to radiate. Although predicted by theory, replicated adaptive radiations occur only rarely, usually in closely related and poorly dispersing taxa found in the same region on islands or in lakes. Contingencies of a variety of types may usually preclude close similarity in the outcome of evolutionary diversification in other situations. Whether radiations usually unfold in the same general sequence is unclear because of the unreliability of methods requiring phylogenetic reconstruction of ancestral events. The synthesis of ecological, phylogenetic, experimental, and genomic advances promises to make the coming years a golden age for the study of adaptive radiation; natural history data, however, will always be crucial to understanding the forces shaping adaptation and evolutionary diversification.

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L. J. Revell, D.L. Mahler, J. R. Sweeney, M. Sobotka, V. E. Fancher, and J. B. Losos. 2010. “Nonlinear selection and the evolution of variances and covariances for continuous characters in an anole.” Journal of Evolutionary Biology, 23: 407-21. Abstract

The pattern of genetic variances and covariances among characters, summarized in the additive genetic variance-covariance matrix, G, determines how a population will respond to linear natural selection. However, G itself also evolves in response to selection. In particular, we expect that, over time, G will evolve correspondence with the pattern of multivariate nonlinear natural selection. In this study, we substitute the phenotypic variance-covariance matrix (P) for G to determine if the pattern of multivariate nonlinear selection in a natural population of Anolis cristatellus, an arboreal lizard from Puerto Rico, has influenced the evolution of genetic variances and covariances in this species. Although results varied among our estimates of P and fitness, and among our analytic techniques, we find significant evidence for congruence between nonlinear selection and P, suggesting that natural selection may have influenced the evolution of genetic constraint in this species.

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L. J. Harmon, J. B. Losos, T. Jonathan Davies, R. G. Gillespie, J. L. Gittleman, W. Bryan Jennings, K. H. Kozak, M. A. McPeek, F. Moreno-Roark, T. J. Near, A. Purvis, R. E. Ricklefs, D. Schluter, J. A. Schulte Ii, O. Seehausen, B. L. Sidlauskas, O. Torres-Carvajal, J. T. Weir, and A. O. Mooers. 2010. “Early bursts of body size and shape evolution are rare in comparative data.” Evolution, 64: 2385-96. Abstract

George Gaylord Simpson famously postulated that much of life's diversity originated as adaptive radiations-more or less simultaneous divergences of numerous lines from a single ancestral adaptive type. However, identifying adaptive radiations has proven difficult due to a lack of broad-scale comparative datasets. Here, we use phylogenetic comparative data on body size and shape in a diversity of animal clades to test a key model of adaptive radiation, in which initially rapid morphological evolution is followed by relative stasis. We compared the fit of this model to both single selective peak and random walk models. We found little support for the early-burst model of adaptive radiation, whereas both other models, particularly that of selective peaks, were commonly supported. In addition, we found that the net rate of morphological evolution varied inversely with clade age. The youngest clades appear to evolve most rapidly because long-term change typically does not attain the amount of divergence predicted from rates measured over short time scales. Across our entire analysis, the dominant pattern was one of constraints shaping evolution continually through time rather than rapid evolution followed by stasis. We suggest that the classical model of adaptive radiation, where morphological evolution is initially rapid and slows through time, may be rare in comparative data.

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M. A. Johnson, L. J. Revell, and J. B. Losos. 2010. “Behavioral convergence and adaptive radiation: effects of habitat use on territorial behavior in Anolis lizards.” Evolution, 64: 1151-9. Abstract

Most studies of adaptive radiations focus on morphological aspects of differentiation, yet behavior is also an important component of evolutionary diversification, often mediating the relationship between animal ecology and morphology. In species within radiations that are convergent in ecology and morphology, we then also expect convergence in behavior. Here, we examined 13 Anolis lizard species to determine whether territorial strategies have evolved convergently with morphology and habitat use. We evaluated two aspects of territoriality: behavioral defense of space via territorial displays, and territory overlap within and between sexes. Controlling for the phylogenetic relationships of the taxa in our study, we found that species similar in perch height and diameter convergently evolved patterns of territory overlap, whereas species similar in habitat visibility (the proportion of space that can be seen from a perch) convergently evolved display behavior. We also found that species with greater display time have more extensive male-male territory overlap. This study provides strong evidence for the role of habitat in the evolution of territoriality and suggests that the social structure of a species ultimately evolves in concert with habitat use and morphology.

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C. G. Willis, B. R. Ruhfel, R. B. Primack, A. J. Miller-Rushing, J. B. Losos, and C. C. Davis. 2010. “Favorable climate change response explains non-native species' success in Thoreau's woods.” PLoS One, 5: e8878. Abstract

Invasive species have tremendous detrimental ecological and economic impacts. Climate change may exacerbate species invasions across communities if non-native species are better able to respond to climate changes than native species. Recent evidence indicates that species that respond to climate change by adjusting their phenology (i.e., the timing of seasonal activities, such as flowering) have historically increased in abundance. The extent to which non-native species success is similarly linked to a favorable climate change response, however, remains untested. We analyzed a dataset initiated by the conservationist Henry David Thoreau that documents the long-term phenological response of native and non-native plant species over the last 150 years from Concord, Massachusetts (USA). Our results demonstrate that non-native species, and invasive species in particular, have been far better able to respond to recent climate change by adjusting their flowering time. This demonstrates that climate change has likely played, and may continue to play, an important role in facilitating non-native species naturalization and invasion at the community level.

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