Publications

Journal Article
T. J. Sanger, L. J. Revell, J. J. Gibson-Brown, and J. B. Losos. 2012. “Repeated modification of early limb morphogenesis programs underlies the convergence of relative limb length in Anolis lizards.” Proceedings of the Royal Society of London, 279, Pp. 739-48.Abstract

The independent evolution of similar morphologies has long been a subject of considerable interest to biologists. Does phenotypic convergence reflect the primacy of natural selection, or does development set the course of evolution by channelling variation in certain directions? Here, we examine the ontogenetic origins of relative limb length variation among Anolis lizard habitat specialists to address whether convergent phenotypes have arisen through convergent developmental trajectories. Despite the numerous developmental processes that could potentially contribute to variation in adult limb length, our analyses reveal that, in Anolis lizards, such variation is repeatedly the result of changes occurring very early in development, prior to formation of the cartilaginous long bone anlagen.

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JB Losos, DM Hillis, and HW Greene. 2012. “Evolution. Who speaks with a forked tongue?.” Science, 338, Pp. 1428-9. PDF
M. Lopez-Darias, T. W. Schoener, D. A. Spiller, and J. B. Losos. 2012. “Predators determine how weather affects the spatial niche of lizard prey: exploring niche dynamics at a fine scale.” EcologyEcologyEcology, 93, Pp. 2512-8.Abstract

Although abiotic and biotic factors can interact to shape the spatial niche of a species, studies that explore the interactive effects of both at a local scale are rare. We demonstrate that one of the main axes (perch height) characterizing the spatial niche of a common lizard, Anolis sagrei, varies according to the interactive effects of weather and the activity of a larger predatory lizard, Leiocephalus carinatus. Results were completely consistent: no matter how favorable the weather conditions for using the ground (mainly characterized by temperature, humidity, wind speed, rain), A. sagrei did not do so if the predator was present. Hence, great behavioral plasticity enabled A. sagrei to adjust its use of space very quickly. To the best of our knowledge, these results constitute the first field demonstration for anoles (and possibly for other animals as well) of how time-varying environmental conditions and predator presence interact to produce short-term changes in utilization along a major niche axis.

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JB Losos. 2012. “Don't jump to conclusions on fraud.” Science, 336, Pp. 412-3. PDF
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, Pp. 1-10. PDF
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, Pp. 1125-1137. PDF
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, Pp. 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, Pp. 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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J. B. Losos. 2011. “Seeing the forest for the trees: the limitations of phylogenies in comparative biology..” American Naturalist, 177, Pp. 709-27.Abstract

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, Pp. E1-2; discussion E3. PDF
J. B. Losos. 2011. “Convergence, adaptation, and constraint.” Evolution, 65, Pp. 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, Pp. 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, Pp. 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, Pp. 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. PDF
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, Pp. 1-22. PDF Supplementary Material
M Leal and JB Losos. 2010. “Evolutionary biology: Communication and speciation.” Nature, 467, Pp. 159-60. PDF
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, Pp. 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, Pp. 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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RB Huey, JB Losos, and C Moritz. 2010. “Are lizards toast?.” Science, 328, Pp. 832-3. PDF

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