A developmental staging series for the lizard genus Anolis: a new system for the integration of evolution, development, and ecology

Vertebrate developmental biologists typically rely on a limited number of model organisms to understand the evolutionary bases of morphological change. Unfortunately, a typical model system for squamates (lizards and snakes) has not yet been developed leaving many fundamental questions about morphological evolution unaddressed. New model systems would ideally include clades, rather than single species, that are amenable to both laboratory studies of development and field-based analyses of ecology and evolution. Combining an understanding of development with an understanding of ecology and evolution within and between closely related species has the potential to create a seamless understanding of how genetic variation underlies ecologically and evolutionarily relevant variation within populations and between species. Here we briefly introduce a new model system for the integration of development, evolution, and ecology, the lizard genus Anolis, a diverse group of lizards whose ecology and evolution is well understood, and whose genome has recently been sequenced. We present a developmental staging series for Anolis lizards that can act as a baseline for later comparative and experimental studies within this genus.     

Hydra and the evolution of stem cells

Hydra are remarkable because they are immortal. Much of immortality can be ascribed to the asexual mode of reproduction by budding, which requires a tissue consisting of stem cells with continuous self‐renewal capacity. Emerging novel technologies and the availability of genomic resources enable for the first time to analyse these cells in vivo. Stem cell differentiation in Hydra is governed through the coordinated actions of conserved signaling pathways. Studies of stem cells in Hydra, therefore, promise critical insights of general relevance into stem cell biology including cellular senescence, lineage programming and reprogramming, the role of extrinsic signals in fate determination and tissue homeostasis, and the evolutionary origin of these cells. With these new facts as a backdrop, this review traces the history of studying stem cells in Hydra and offers a view of what the future may hold.     

The uropygial gland of the monk parakeet Myiopsitta monachus: Histology,morphogenesis, and evolution within Psittaciformes (Aves)

We describe the morphology, histology, and histochemical characteristics of the uropygial gland (UG) of the monk parakeet Myiopsitta monachus. The UG has a heart‐shape external appearance and adenomers extensively branched with a convoluted path, covered by a stratified epithelium formed by different cellular strata and divided into three zones (based on the epithelial height and lumen width), a cylindrical papilla with an internal structure of delicate type and two excretory pores surrounded by a feather tuft. Histochemical and lectin‐histochemical techniques performed showed positivity against PAS, AB pH 2.5, AB‐PAS, and some lectines, likely related to the granivorous feeding habits. Also, we describe the morphogenesis of the UG of the monk parakeet, which appears at embryological stage 34 as a pair of ectodermal invaginations. Heterochronic events in the onset development of the UG when compared with other birds could be recognized. Finally, to examine the phylogenetic occurrence of the UG within the Psittaciformes and infer its evolutionary history, we mapped its presence/absence over a molecular phylogeny. The reconstruction of the characters states at ancestral nodes revealed that the presence of the UG was the plesiomorphic feature for Psittaciformes and its loss evolved independently more than once.     

The evolutionary and morphological history of the parasphenoid bone in vertebrates

The parasphenoid is located in the cranium of many vertebrates. When present, it is always an unpaired, dermal bone. While most basal vertebrates have a parasphenoid, most placental mammals lack this element and have an unpaired, dermal vomer in a similar position (i.e. associated with the same bones) and with a similar function. As such, the parasphenoid and the vomer were considered homologous by some early twentieth century researchers. However, others questioned this homology based on comparisons between mammals and reptiles. Here we investigate the parasphenoid bone across the major vertebrate lineages (amphibians, reptiles, mammals and teleosts) including both developmental and evolutionary aspects, which until now have not been considered together. We find that within all the major vertebrate lineages there are organisms that possess a parasphenoid and a vomer, while the parasphenoid is absent within caecilians and most placental mammals. Based on our assessment and Patterson's conjunction tests, we conclude that the non‐mammalian parasphenoid and the vomer in mammals cannot be considered homologous. Additionally, the parasphenoid is likely homologous between sarcopterygian and actinopterygian lineages. This research attempts to resolve the issue of the parasphenoid homology and highlights where gaps in our knowledge are still present.     

Genes,development, and evolvability in primate evolution

Development is the process whereby a fertilized cell becomes a mature individual. In metazoans, this complex process involves the differentiation of somatic cells into committed cell and tissue types; the organization and migration of cells, tissues, and anatomical structures relative to one another; and growth. 1 Development matters to evolution in two ways. First, development carries out heritable genetic instructions contained in zygotes to produce functioning yet phenotypically varied individuals. At the population level, this variation in form and function among individuals provides the “raw material” for evolution. Second, the mechanisms of development influence the magnitude, direction, and interdependence of heritable phenotypic variation among traits. Together with phenomena such as genetic drift, organismal development determines the raw material available to selection and thus influences the rate and direction of phenotypic evolution. 2 , 3     

The oestrogen pathway underlies the evolution of exaggerated male cranial shapes in Anolis lizards

Sexual dimorphisms vary widely among species. This variation must arise through sex-specific evolutionary modifications to developmental processes. Anolis lizards vary extensively in their expression of cranial dimorphism. Compared with other Anolis species, members of the carolinensis clade have evolved relatively high levels of cranial dimorphism; males of this clade have exceptionally long faces relative to conspecific females. Developmentally, this facial length dimorphism arises through an evolutionarily novel, clade-specific strategy. Our analyses herein reveal that sex-specific regulation of the oestrogen pathway underlies evolution of this exaggerated male phenotype, rather than the androgen or insulin growth factor pathways that have long been considered the primary regulators of male-biased dimorphism among vertebrates. Our results suggest greater intricacy in the genetic mechanisms that underlie sexual dimorphisms than previously appreciated.     

How a growing organismal perspective is adding new depth to integrative studies of morphological evolution

Over the past half century, the field of Evolutionary Developmental Biology, or Evo‐devo, has integrated diverse fields of biology into a more synthetic understanding of morphological diversity. This has resulted in numerous insights into how development can evolve and reciprocally influence morphological evolution, as well as generated several novel theoretical areas. Although comparative by default, there remains a great gap in our understanding of adaptive morphological diversification and how developmental mechanisms influence the shape and pattern of phenotypic variation. Herein we highlight areas of research that are in the process of filling this void, and areas, if investigated more fully, that will add new insights into the diversification of morphology. At the centre of our discussion is an explicit awareness of organismal biology. Here we discuss an organismal framework that is supported by three distinct pillars. First, there is a need for Evo‐devo to adopt a high‐resolution phylogenetic approach in the study of morphological variation and its developmental underpinnings. Secondly, we propose that to understand the dynamic nature of morphological evolution, investigators need to give more explicit attention to the processes that generate evolutionarily relevant variation at the population level. Finally, we emphasize the need to address more thoroughly the processes that structure variation at micro‐ and macroevolutionary scales including modularity, morphological integration, constraint, and plasticity. We illustrate the power of these three pillars using numerous examples from both invertebrates and vertebrates to emphasize that many of these approaches are already present within the field, but have yet to be formally integrated into many research programs. We feel that the most exciting new insights will come where the traditional experimental approaches to Evo‐devo are integrated more thoroughly with the principles of this organismal framework.     

Patterns of ecomorphological convergence among mainland and island Anolis lizards

Differing selective pressures on islands versus the mainland may produce alternative evolutionary outcomes among closely related lineages. Conversely, lineages may be constrained to produce similar outcomes in different mainland and island environments, or mainland and island environments may not differ significantly. Among the best‐studied island radiations are Caribbean Anolis lizards. Distinct morphotypes, or ‘ecomorphs’, have been described, and the same ecomorphs have evolved independently on each Greater Antillean island. The mainland Anolis radiation has received much less attention. We use a large morphological data set and a novel phylogenetic hypothesis to show that mainland Anolis did not evolve the same morphotypes as island Anolis, despite some island species being more closely related to mainland species than to island species that share their morphotype. A maximum of four of the six Caribbean ecomorphs were found to exist on the mainland, and just 15 of 123 mainland species are assignable to a Caribbean ecomorph. This result was insensitive to differing taxon samples and alternative phylogenetic hypotheses. Mainland convergence to a Caribbean ecomorph occurs only among species assigned to the grass‐bush ecomorph. Thus, the ecomorphs that have evolved convergently multiple times in the Caribbean have not evolved in parallel on the mainland. These results are consistent with the hypothesis that mainland and island environments offer different selective pressures. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 852–859.     

The evolution of teleost pigmentation and the fish‐specific genome duplication

Teleost fishes have evolved a unique complexity and diversity of pigmentation and colour patterning that is unmatched among vertebrates. Teleost colouration is mediated by five different major types of neural‐crest derived pigment cells, while tetrapods have a smaller repertoire of such chromatophores. The genetic basis of teleost colouration has been mainly uncovered by the cloning of pigmentation genes in mutants of zebrafish Danio rerio and medaka Oryzias latipes. Many of these teleost pigmentation genes were already known as key players in mammalian pigmentation, suggesting partial conservation of the corresponding developmental programme among vertebrates. Strikingly, teleost fishes have additional copies of many pigmentation genes compared with tetrapods, mainly as a result of a whole‐genome duplication that occurred 320–350 million years ago at the base of the teleost lineage, the so‐called fish‐specific genome duplication. Furthermore, teleosts have retained several duplicated pigmentation genes from earlier rounds of genome duplication in the vertebrate lineage, which were lost in other vertebrate groups. It was hypothesized that divergent evolution of such duplicated genes may have played an important role in pigmentation diversity and complexity in teleost fishes, which therefore not only provide important insights into the evolution of the vertebrate pigmentary system but also allow us to study the significance of genome duplications for vertebrate biodiversity.     

Multilevel assessment of the Lacertid lizard cranial modularity

Different factors and processes that produce phenotypic variation at the individual, population, or interspecific level can influence or alter the covariance structure among morphological traits. Therefore, studies of the patterns of integration and modularity at multiple levels—static, ontogenetic, and evolutionary, can provide invaluable data on underlying factors and processes that structured morphological variation, directed, or constrained evolutionary changes. Our dataset, consisting of cranium shape data for 14 lizard species from the family Lacertidae, with substantial samples of hatchlings and adults along with their inferred evolutionary relationships, enabled us to assess modularity and morphological integration at all three levels. Five, not mutually exclusive modularity hypotheses of lizard cranium, were tested, and the effects of allometry on intensity and the pattern of integration and modularity were estimated. We used geometric morphometrics to extract symmetric and asymmetric, as well as allometric and nonallometric, components of shape variation. At the static level, firm confirmation of cranial modularity was found for hypotheses which separate anterior and posterior functional compartments of the skull. At the ontogenetic level, two alternative hypotheses (the “anteroposterior” and “neurodermatocranial” hypotheses) of ventral cranial modularity were confirmed. At the evolutionary level, the “neurodermatocranial” hypothesis was confirmed for the ventral cranium, which is in accordance with the pattern observed at the ontogenetic level. The observed pattern of static modularity could be driven by functional demands and can be regarded as adaptive. Ontogenetic modularity and evolutionary modularity show the same developmental origin, indicating conservatism of modularity patterns driven by developmental constraints.     

Repeated evolution of underwater rebreathing in diving Anolis lizards

1. Download : Download high-res image (182KB)
2. Download : Download full-size image

     

Testing the island effect in adaptive radiation: rates and patterns of morphological diversification in Caribbean and mainland Anolis lizards

Many of the classic examples of adaptive radiation, including Caribbean Anolis lizards, are found on islands. However, Anolis also exhibits substantial species richness and ecomorphological disparity on mainland Central and South America. We compared patterns and rates of morphological evolution to investigate whether, in fact, island Anolis are exceptionally diverse relative to their mainland counterparts. Quite the contrary, we found that rates and extent of diversification were comparable--Anolis adaptive radiation is not an island phenomenon. However, mainland and Caribbean anoles occupy different parts of morphological space; in independent colonizations of both island and mainland habitats, island anoles have evolved shorter limbs and better-developed toe pads. These patterns suggest that the two areas are on different evolutionary trajectories. The ecological causes of these differences are unknown, but may relate to differences in predation or competition among mainland and island communities.     

Parallel reduction in expression of the eye development gene hedgehog in separately derived cave populations of the amphipod Gammarus minus

Caves provide excellent settings to examine evolutionary questions. Subterranean environments are characterized by similar and consistent conditions. Cave-adapted species often share characteristics such as diminished pigmentation, elongated limbs and reduced or absent eyes. Relatively little is known about the evolution and development of troglomorphic traits in invertebrates. In this study, we compare expression of the eye development genes hedgehog, pax6, sine oculis and dachshund in individuals from multiple independently derived cave populations of the amphipod Gammarus minus. hedgehog expression was significantly reduced in cave populations, compared to genetically related surface populations. Interestingly, no differences were found in pax6, sine oculis or dachshund expression. Because hedgehog-related genes are also involved in eye reduced in Astyanax mexicanus, these genes may be consistent targets of evolution during cave adaptation. These results provide support for the hypothesis of genomic 'hotspots' of evolution and allow comparison of adaptive mechanisms among diverse animals in subterranean environments.     

Evolutionary stasis in Euphorbiaceae pollen: selection and constraints

Although much attention has been paid to the role of stabilizing selection, empirical analyses testing the role of developmental constraints in evolutionary stasis remain rare, particularly for plants. This topic is studied here with a focus on the evolution of a pollen ontogenetic feature, the last points of callose deposition (LPCD) pattern, involved in the determination of an adaptive morphological pollen character (aperture pattern). The LPCD pattern exhibits a low level of evolution in eudicots, as compared to the evolution observed in monocots. Stasis in this pattern might be explained by developmental constraints expressed during male meiosis (microsporogenesis) or by selective pressures expressed through the adaptive role of the aperture pattern. Here, we demonstrate that the LPCD pattern is conserved in Euphorbiaceae s.s. and that this conservatism is primarily due to selective pressures. A phylogenetic association was found between the putative removal of selective pressures on pollen morphology after the origin of inaperturate pollen, and the appearance of variation in microsporogenesis and in the resulting LPCD pattern, suggesting that stasis was due to these selective pressures. However, even in a neutral context, variation in microsporogenesis was biased. This should therefore favour the appearance of some developmental and morphological phenotypes rather than others.     

The role of inhibitory dynamics in the loss and reemergence of macropodoid tooth traits

The reversibility of phenotypic evolution is likely to be strongly influenced by the ability of underlying developmental systems to generate ancestral traits. However, few studies have quantitatively linked these developmental dynamics to traits that reevolve. In this study, we assess how changes in the inhibitory cascade, a developmental system that regulates relative tooth size in mammals, influenced the loss and reversals of the posthypocristid, a molar tooth crest, in the kangaroo superfamily Macropodoidea. We find that posthypocristid loss is linked with reduced levels of posterior molar inhibition, potentially driven by selection for lophodont, higher‐crowned molar teeth. There is strong support for two posthypocristid reversals, each occurring after more than 15 million years of absence, in large‐bodied species of Macropus, and two giant extinct species of short‐faced sthenurine kangaroo (Procoptodon). We find that whereas primitive posthypocristid expression is linked to higher levels of posterior molar inhibition, reemergence is tied to a relative increase in third molar size associated with increasing body mass, producing molar phenotypes similar to those in mouse where the ectodysplasin pathway is upregulated. We argue that although shifts in the inhibitory cascade may enable reemergence, dietary ecology may limit the frequency of phylogenetic reversal.