HOW LIZARDS TURN INTO SNAKES: A PHYLOGENETIC ANALYSIS OF BODY-FORM EVOLUTION IN ANGUID LIZARDS

Abstract One of the most striking morphological transformations in vertebrate evolution is the transition from a lizardlike body form to an elongate, limbless (snakelike) body form. Despite its dramatic nature, this transition has occurred repeatedly among closely related species (especially in squamate reptiles), making it an excellent system for studying macroevolutionary transformations in body plan. In this paper, we examine the evolution of body form in the lizard family Anguidae, a clade in which multiple independent losses of limbs have occurred. We combine a molecular phylogeny for 27 species, our morphometric data, and phylogenetic comparative methods to provide the first statistical phylogenetic tests of several long‐standing hypotheses for the evolution of snakelike body form. Our results confirm the hypothesized relationships between body elongation and limb reduction and between limb reduction and digit reduction. However, we find no support for the hypothesized sequence going from body elongation to limb reduction to digit loss, and we show that a burrowing lifestyle is not a necessary correlate of limb loss. We also show that similar degrees of overall body elongation are achieved in two different ways in anguids, that these different modes of elongation are associated with different habitat preferences, and that this dichotomy in body plan and ecology is widespread in limb‐reduced squamates. Finally, a recent developmental study has proposed that the transition from lizardlike to snakelike body form involves changes in the expression domains of midbody Hox genes, changes that would link elongation and limb loss and might cause sudden transformations in body form. Our results reject this developmental model and suggest that this transition involves gradual changes occurring over relatively long time scales.     

A PHYLOGENETIC ANALYSIS OF CHARACTER DISPLACEMENT IN CARIBBEAN ANOLIS LIZARDS

Twenty-seven islands in the Lesser Antilles contain either one or two species of Anolis lizards. On nine of the ten two-species islands, the species differ substantially in size; 16 of the 17 one-species islands harbor an intermediate-sized species. Two processes could produce such a pattern: size adjustment (or character displacement), in which similar-sized species evolve in different directions in sympatry; and size assortment, in which only different-sized species can successfully colonize the same island together. Previous analyses implicitly have assumed that size is evolutionarily plastic and determined solely by recent ecological conditions, and consequently have tested the hypothesis that character displacement has occurred on each of the ten two-species islands. Other studies have focused only on size assortment. By analyzing such patterns in a phylogenetic context, I explicitly consider historical effects and can distinguish between size adjustment and size assortment. Using a minimum evolution algorithm, I assess evidence for size adjustment by partitioning changes in size along branches of the phylogenetic tree. Size evolution appears rare (a minimum of 4-7 instances of substantial size evolution). In the northern (but not the southern) Lesser Antilles, size change was significantly greater when a descendant taxon occurred on a two-species island and its hypothetical ancestor occurred on a one-species island, thus supporting the size adjustment hypothesis, though size adjustment might have occurred only once. The relative rarity of size evolution suggests that size assortment might be responsible for nonrandom patterns. In both the northern and southern Lesser Antilles, a null model of no size assortment is convincingly rejected. Closely related taxa, however, are usually similar in size, and hybridization between species has been reported. Consequently, similar-sized species might not coexist because they interbreed and coalesce into one gene pool. A null model that only allows species from different “clades” to co-occur is rejected for the northern Lesser Antilles, but is ambiguous with regard to the southern Lesser Antilles. Thus, competitive exclusion is probably responsible for the pattern of size assortment in the northern Lesser Antilles; both competitive exclusion and interbreeding of closely related species of similar size might be responsible for the patterns evident in the southern Lesser Antilles.     

PHYLOGENETIC STUDIES OF THE GENUSARTHONIA

A phylogenetic analysis is presented, based on 57 morphological, anatomical, chemical and ecological characters, including 19 species from the generaArthonia,ArthotheliumandSyncesia. The aim of the study was to test the monophyly of some of the groups within the genusArthoniasuggested, for example, by Redinger (e.g. species with reddish ascomata, with grey–pruinose ascomata and with brown–black hypothecia). The results strongly support thatArthoniaandArthotheliumare paraphyletic genera. The best-supported node contains allArthoniaspecies together withA. crozalsianade Lesd.,A. ruanaA. Massal. (both hitherto placed inArthothelium) andSyncesia myrticola(Fée) Tehler. A well-supported clade is formed by a group of pioneer species, often non-lichenized or poorly lichenized, including the type species ofArthonia,A. radiata. The species with reddish and/or K+ reddish ascomata form one clade and the species with more or less brownish or blackish hypothecia form another clade withSyncesia myrticola, the sister group to theOpegraphaceaeandRoccellaceae. The results are discussed and compared with Redinger’s grouping. Relationships to other genera within Arthoniaceae are briefly discussed.Arthothelium scandinavicumTh. Fr.,Arthonia dispersa(Schrad.) Nyl.,A. punctiformisAch. andA. mediellaNyl. are lectotypified.     

EVOLUTION OF VIVIPARITY: A PHYLOGENETIC TEST OF THE COLD‐CLIMATE HYPOTHESIS IN PHRYNOSOMATID LIZARDS

The evolution of viviparity is a key life‐history transition in vertebrates, but the selective forces favoring its evolution are not fully understood. With >100 origins of viviparity, squamate reptiles (lizards and snakes) are ideal for addressing this issue. Some evidence from field and laboratory studies supports the “cold‐climate” hypothesis, wherein viviparity provides an advantage in cold environments by allowing mothers to maintain higher temperatures for developing embryos. Surprisingly, the cold‐climate hypothesis has not been tested using both climatic data and phylogenetic comparative methods. Here, we investigate the evolution of viviparity in the lizard family Phrynosomatidae using GIS‐based environmental data, an extensive phylogeny (117 species), and recently developed comparative methods. We find significant relationships between viviparity and lower temperatures during the warmest (egg‐laying) season, strongly supporting the cold‐climate hypothesis. Remarkably, we also find that viviparity tends to evolve more frequently at tropical latitudes, despite its association with cooler climates. Our results help explain this and two related patterns that seemingly contradict the cold‐climate hypothesis: the presence of viviparous species restricted to low‐elevation tropical regions and the paucity of viviparous species at high latitudes. Finally, we examine whether viviparous taxa may be at higher risk of extinction from anthropogenic climate change.     

EVOLUTIONARY STUDIES OF ATRIPLEX: PHYLOGENETIC RELATIONSHIPS OF ATRIPLEX PLEIANTHA

Atriplex pleiantha Weber differs from all other species of Atriplex in having 1) multiple female flowers subtended by two bracts, 2) female flowers with a perianth, and 3) embryos with radicles pointing downwards. Because of these significant differences it is proposed that Atriplex pleiantha be elevated to the level of a separate genus and be designated Proatriplex pleiantha (Weber) Stutz & Chu. The closest relatives of Proatriplex appear to be Archiatriplex, Endolepis, Exomis, and Microgynoecium. These are all diploid, monoecious annuals, have non-Kranz type leaf anatomy, and female flowers with a perianth.     

THE EVOLUTION OF OVIPARITY WITH EGG GUARDING AND VIVIPARITY IN LIZARDS AND SNAKES: A PHYLOGENETIC ANALYSIS

This paper investigates the evolution of viviparity and of egg guarding in lizards and snakes in which three modes of reproduction can be described: oviparity without egg guarding, oviparity with egg guarding, and viviparity. All possible transitions of reproductive modes were detected in each taxon using Maddison's method. We then tested two specific hypotheses. First, egg guarding can be regarded as an alternative to viviparity. A relatively frequent association of egg guarding and viviparous species in the same taxon may be due to similar environmental conditions or species characteristics leading to two different solutions. Second, egg guarding may facilitate the evolution of viviparity. This hypothesis is supported by the high frequency of viviparous species in taxa containing egg guarding species and by a tendency for prolonged uterine retention of eggs in brooding squamates. Our analyses demonstrate that the first hypothesis is the best supported. Egg guarding and viviparity most often evolved independently. If a major benefit of egg guarding is the repulsion of potential predators, size is one of the most obvious morphological characters that should be correlated with the evolution of reproductive modes. The two reproductive traits were correlated to a reduction in body size for viviparous species and an increase in body size for egg guarding species. This could partly explain why the evolution of these reproductive modes seems almost antagonist.     

A COMPARATIVE ANALYSIS OF THE ECOLOGICAL SIGNIFICANCE OF MAXIMAL LOCOMOTOR PERFORMANCE IN CARIBBEAN ANOLIS LIZARDS

We examined the sprinting and jumping capabilities of eight West Indian Anolis species during three natural activities (escape from a predator, feeding, and undisturbed activity). We then compared these field data with maximal performance under optimal laboratory conditions to answer three questions: (1) Has maximal (i.e., laboratory) sprinting and jumping performance coevolved with field performance among species? (2) What proportion of their maximum capabilities do anoles sprint and jump in different ecological contexts? (3) Does a relationship exist between maximal sprinting and jumping ability and the proportion of maximal performance used in these contexts? Among species, maximal speed is tightly positively correlated with sprinting performance during both feeding and escape in the field. Sprinting speed during escape closely matches maximal sprinting ability (i.e., about 90% of maximum performance). By contrast, sprinting performance during undisturbed activity is markedly lower (about 32% of maximum) than maximal sprinting performance. Sprinting ability during feeding is intermediate (about 71% of maximum) between field escape and field undisturbed activity. In contrast to sprinting ability, jumping ability is always substantially less than maximum (about 40% of maximum during feeding and undisturbed activity). A negative relationship exists among species between maximal speed and the proportion to which species sprint to their maximal abilities during field escape.     

THE EVOLUTION OF FORM AND FUNCTION: MORPHOLOGY AND LOCOMOTOR PERFORMANCE IN WEST INDIAN ANOLIS LIZARDS

I tested biomechanical predictions that morphological proportions (snout–vent length, forelimb length, hindlimb length, tail length, and mass) and maximal sprinting and jumping ability have evolved concordantly among 15 species of Anolis lizards from Jamaica and Puerto Rico. Based on a phylogenetic hypothesis for these species, the ancestor reconstruction and contrast approaches were used to test hypotheses that variables coevolved. Evolutionary change in all morphological and performance variables scales positively with evolution of body size (represented by snout–vent length); size evolution accounts for greater than 50% of the variance in sprinting and jumping evolution. With the effect of the evolution of body size removed, increases in hindlimb length are associated with increases in sprinting and jumping capability. When further variables are removed, evolution in forelimb and tail length exhibits a negative relationship with evolution of both performance measures. The success of the biomechanical predictions indicates that the assumption that evolution in other variables (e.g., muscle mass and composition) did not affect performance evolution is probably correct; evolution of the morphological variables accounts for approximately 80% of the evolutionary change in performance ability. In this case, however, such assumptions are clade-specific; extrapolation to taxa outside the clade is thus unwarranted. The results have implications concerning ecomorphological evolution. The observed relationship between forelimb and tail length and ecology probably is a spurious result of the correlation between these variables and hindlimb length. Further, because the evolution of jumping and sprinting ability are closely linked, the ability to adapt to certain microhabitats may be limited.     

羧甲基淀粉崩解性能研究

本研究考察了崩解剂羧甲基淀粉（ＣＭＳ）的取代度（ＤＳ）和ＣＭＳ中Ｈ／Ｎａ（游离羧基和成盐羧基比值）改变对其吸水溶胀性能和崩解性能的影响。并应用红外光谱,Ｘ－射线衍射和扫描电镜等方法探求ＣＭＳ的结构与性能的关系。     

POOR STATISTICAL PERFORMANCE OF THE MANTEL TEST IN PHYLOGENETIC COMPARATIVE ANALYSES

The Mantel test, based on comparisons of distance matrices, is commonly employed in comparative biology, but its statistical properties in this context are unknown. Here, we evaluate the performance of the Mantel test for two applications in comparative biology: testing for phylogenetic signal, and testing for an evolutionary correlation between two characters. We find that the Mantel test has poor performance compared to alternative methods, including low power and, under some circumstances, inflated type‐I error. We identify a remedy for the inflated type‐I error of three‐way Mantel tests using phylogenetic permutations; however, this test still has considerably lower power than independent contrasts. We recommend that use of the Mantel test should be restricted to cases in which data can only be expressed as pairwise distances among taxa.     

中国慈姑属系统发育的研究

本文研究了中国慈姑属植物间的系统发育关系。选取了12个与该属系统发育有较重要关系的特征,将8个已知分类群与外类群刺果泽泻属进行了比较。应用数量分支分析的Farris-Wagner方法,建立了中国慈姑属系统发育分支图。讨论了各分类群间的系统发育关系、该属起源和数量分支分析方法等问题。     

STUDIES OF PALEOZOIC MARATTIALEANS: THE MORPHOLOGY AND PHYLOGENETIC POSITION OF EOANGIOPTERIS GOODII SP. N.

Eoangiopteris goodii sp. n. is described from Upper Pennsylvanian coal balls from Ohio (Shade locality) containing isolated pecopterid pinnules approx. 7 × 9 mm that bear up to 20 linear synangia on the lower surface. The synangia extend at right angles from the midrib to the downturned pinnule margins and measure 2.0–3.5 mm in length. Individual synangia are compact and are composed of 10–19 sporangia that have their bases embedded in an elongate parenchymatous pad. In longitudinal section sporangia measure 0.4 × 2.0 mm and have acute elongate, curved apices. Spores average 70 μm in diam and are most similar to the dispersed spore genus Verrucosisporites. Eoangiopteris goodii differs from the generitype E. andrewsii Mamay in its greater size, pinnule histology, and spore type. Sporangium wall complexity and spore type of the two presently known species of Eoangiopteris are considered to be at about the same evolutionary level as the more primitive species of Scolecopteris. Construction of the synangia in Eoangiopteris is different from that of Scolecopteris and indicates that at least two evolutionary lines are recognizable within the Pennsylvanian Marattiales.     

THE EVOLUTION OF MATERNAL INVESTMENT IN LIZARDS: AN EXPERIMENTAL AND COMPARATIVE ANALYSIS OF EGG SIZE AND ITS EFFECTS ON OFFSPRING PERFORMANCE

I used comparative and experimental analysis of egg size in a Sceloporus lizard to examine a fundamental tenet of life-history theory: the presumed trade-offs among offspring number, offspring size, and performance traits related to offspring size that are likely to influence fitness. I analyzed latitudinal and elevational patterns of egg life-history characteristics among populations and experimentally manipulated egg size and hatchling size by removing yolk from the eggs to examine the causal bases of population differences in offspring traits. Mean clutch size among populations increased to the north (seven vs. 12 eggs/clutch, California vs. Washington), whereas egg size decreased (0.65 g vs. 0.40 g). The elevational patterns in southern California paralleled the latitudinal trends. Several offspring life-history traits that are correlated with egg size also varied geographically; these traits included incubation time, hatchling size, growth rate, and hatchling sprint performance. Hatchling viability of experimentally reduced eggs was remarkably high (~70%), even when up to 50% of the yolk was removed. The experimentally reduced eggs and hatchlings demonstrated the degree to which size influences each of the offspring life-history traits considered. Northern eggs hatched sooner, in part because of their small size. Though growth rate is allometrically related to size within each population (i.e., smaller hatchlings grow faster on a mass-specific basis), population differences in growth rate, as measured in the laboratory, are likely to reflect genetic differentiation in the underlying physiology of growth. Moreover, smaller juveniles, because of experimental reduction, had slower sprint speeds than larger juveniles. The slower sprint speed of hatchlings from Washington compared to hatchlings from California is thus largely due to the fact that eggs are smaller in the Washington population. These results provide a basis for interpreting the evolutionary divergence of the suite of traits involved in the evolution of maternal investment per offspring in lizards. For example, evolutionary divergence in some offspring traits functionally related to size (e.g., sprint speed) may be constrained, relative to traits that are determined by other aspects of development or physiology (e.g., growth). I also discuss issues relating to the evolution of maternal investment that could be tested in laboratory and natural populations using experimentally reduced offspring.     

A PHYLOGENETIC PERSPECTIVE ON THE EVOLUTION OF SEXUAL DICHROMATISM IN TANAGERS (THRAUPIDAE): THE ROLE OF FEMALE VERSUS MALE PLUMAGE

The evolution of sexual dichromatism in tanagers (family Thraupidae) was studied from a phylogenetic perspective using a molecular-based phylogeny. Mapping patterns of sexual dimorphism in plumage onto the phylogeny reveals that changes in female plumage occur more frequently than changes in male plumage. Possible explanations for this pattern include sexual selection acting on female plumage and natural selection for background matching. The results of this study and other recent phylogenetic and comparative studies suggest that factors affecting female plumage are important in shaping patterns of sexual dimorphism.     

BODY SIZE OF INSULAR LIZARDS: A PATTERN OF HOLOCENE DWARFISM

Until recently there have been scant historical data available to test and supplement studies on the evolution of body size within insular lizards. However, there is now an accumulating fossil record from islands which shows that numerous species have declined in average maximum body size since the beginning of the Holocene, regardless of phylogenetic afffinities, habits, or even size of the species itself. Coincident with decline in body size, human colonization of islands has permanently altered insular environments, with the consequence that native flora and fauna have been depleted. Indeed, the fossil record documents high extinction rates among insular vertebrates during the past few thousand years. It follows that resource deterioration may have led to the reduction of lizard body size, as expressed genotypically in selection for corresponding smaller dimensions, and phenotypically through arrested growth and development leading to compression of the age-class structure. The effect of human settlement on small islands has been underestimated, and although the consequences do not render completely in vain the attempts to understand ecological processes on them, they are of sufficient magnitude to stress caution in any assessment of a modern insular biota.     

USE OF RIBOSOMAL DNA INTERNAL TRANSCRIBED SPACERS FOR PHYLOGENETIC STUDIES IN DIATOMS1

Sequence variation of ribosomal DNA internal transcribed spacers (ITS) among populations, species, and genera of the diatom genus Stephanodiscus was investigated. ITS 1 and ITS 2, including the 5.8S gene, were sequenced from geographically distant and nearby populations of S. niagarae Ehrenberg. In addition, repeats from S. hantzschii Grunow and Cyclotella meneghiniana Kützing were sequenced to determine the taxonomic range over which the ITS region could be used for diatom systematics. The morphologically distinct S. yellowstonensis Theriot & Stoermer, thought to have evolved from S. niagarae in Yellowstone Lake between 12,000 and 8000 years ago, also was sequenced to assess its relationship to nearby S. niagarae populations. The organization and relative sizes of ITS 1 and ITS 2 in Stephanodiscus species were similar to those reported for other eukaryotes. In general, ITS 2 was slightly larger and more variable than ITS 1. Cladistic analysis of ITS sequences did not resolve relationships of nearby S. niagarae and S. yellowstonensis populations. However, central North American S. niagarae populations were in a clade supported by two nucleotide changes. For Cyclotella, much of the ITS region was not alignable with that for Stephanodiscus species; therefore, generic-level comparison within the Thalassiosiraceae may not be possible. The variation (95–96% similarity) between S. hantzschii and other Stephanodiscus species suggests that interspecific relationships could be assessed with ITS sequences. Although S. yellowstonensis is morphologically distinct from S. niagarae, no autapomorphic nucleotide sites were identified. Two S. niagarae populations (Heart and Lewis Lakes), however, did possess autapomorphic ITS sites.