PARALLEL RACE FORMATION AND THE EVOLUTION OF MIMICRY IN HELICONIUS BUTTERFLIES: A PHYLOGENETIC HYPOTHESIS FROM MITOCHONDRIAL DNA SEQUENCES

Mimicry has been a fundamental focus of research since the birth of evolutionary biology yet rarely has been studied from a phylogenetic perspective beyond the simple recognition that mimics are not similar due to common descent. The difficulty of finding characters to discern relationships among closely related and convergent taxa has challenged systematists for more than a century. The phenotypic diversity of wing pattens among mimetic Heliconius adds an additional twist to the problem, because single species contain more than a dozen radically different-looking geographical races even though the mimetic advantage is theoretically highest when all individuals within and between species appear the same. Mitochondrial DNA (mtDNA) offers an independent way to address these issues. In this study, Cytochrome Oxidase I and II sequences from multiple, parallel races of Heliconius erato and Heliconius melpomene are examined, to estimate intraspecific phylogeny and gauge sequence divergence and ages of clades among races within each species. Although phenotypes of sympatric races exhibit remarkable concordance between the two species, the mitochondrial cladograms show that the species have not shared a common evolutionary history. H. erato exhibits a basal split between trans- and cis-Andean groups of races, whereas H. melpomene originates in the Guiana Shield. Diverse races in either species appear to have evolved within the last 200,000 yr, and convergent phenotypes have evolved independently within as well as between species. These results contradict prior theories of the evolution of mimicry based on analysis of wing-pattern genetics.     

REVISING A CLASSIC BUTTERFLY MIMICRY SCENARIO: DEMONSTRATION OF MÜLLERIAN MIMICRY BETWEEN FLORIDA VICEROYS (LIMENITIS ARCHIPPUS FLORIDENSIS) AND QUEENS (DANAUS GILIPPUS BERENICE)

Batesian and Müllerian mimicry relationships differ greatly in terms of selective pressures affecting the participants; hence, accurately characterizing a mimetic interaction is a crucial prerequisite to understanding the selective milieux of model, mimic, and predator. Florida viceroy butterflies (Limenitis archippus floridensis) are conventionally characterized as palatable Batesian mimics of distasteful Florida queens (Danaus gilippus berenice). However, recent experiments indicate that both butterflies are moderately distasteful, suggesting they may be Müllerian comimics. To directly test whether the butterflies exemplify Müllerian mimicry, I performed two reciprocal experiments using red-winged blackbird predators. In Experiment 1, each of eight birds was exposed to a series of eight queens as “models,” then offered four choice trials involving a viceroy (the putative “mimic”) versus a novel alternative butterfly. If mimicry was effective, viceroys should be attacked less than alternatives. I also compared the birds' reactions to solo viceroy “mimics” offered before and after queen models, hypothesizing that attack rate on the viceroy would decrease after birds had been exposed to queen models. In Experiment 2, 12 birds were tested with viceroys as models and queens as putative mimics. The experiments revealed that (1) viceroys and queens offered as models were both moderately unpalatable (only 16% entirely eaten), (2) some birds apparently developed conditioned aversions to viceroy or queen models after only eight exposures, (3) in the subsequent choice trials, viceroy and queen “mimics” were attacked significantly less than alternatives, and (4) solo postmodel mimics were attacked significantly less than solo premodel mimics. Therefore, under these experimental conditions, sampled Florida viceroys and queens are comimics and exemplify Müllerian, not Batesian, mimicry. This compels a reassessment of selective forces affecting the butterflies and their predators, and sets the stage for a broader empirical investigation of the ecological and evolutionary dynamics of mimicry.     

IMMUNE EVASION AND THE EVOLUTION OF MOLECULAR MIMICRY IN PARASITES

Parasites that are molecular mimics express proteins which resemble host proteins. This resemblance facilitates immune evasion because the immune molecules with the specificity to react with the parasite also cross‐react with the host's own proteins, and these lymphocytes are rare. Given this advantage, why are not most parasites molecular mimics? Here we explore potential factors that can select against molecular mimicry in parasites and thereby limit its occurrence. We consider two hypotheses: (1) molecular mimics are more likely to induce autoimmunity in their hosts, and hosts with autoimmunity generate fewer new infections (the “costly autoimmunity hypothesis”); and (2) molecular mimicry compromises protein functioning, lowering the within‐host replication rate and leading to fewer new infections (the “mimicry trade‐off hypothesis”). Our analysis shows that although both hypotheses may select against molecular mimicry in parasites, unique hallmarks of protein expression identify whether selection is due to the costly autoimmunity hypothesis or the mimicry trade‐off hypothesis. We show that understanding the relevant selective forces is necessary to predict how different medical interventions will affect the proportion of hosts that experience the different infection types, and that if parasite evolution is ignored, interventions aimed at reducing infection‐induced autoimmunity may ultimately fail.     

EVOLUTION OF MIMICRY PATTERNS IN METRIORRHYNCHUS (COLEOPTERA: LYCIDAE): THE HISTORY OF DISPERSAL AND SPECIATION IN SOUTHEAST ASIA

The concept of Müllerian mimicry suggests convergent evolution to an intermediate pattern and does not predict polymorphism in mimicry rings. We examined the evolution of mimicry patterns and the order of divergence of various factors, including the role of aposematic patterns in speciation, in a clade of net-winged beetles with a robust phylogeny that suggests that they dispersed from the Australian to Asian plate. We found strong evidence for the evolution of mimicry via advergence in Metriorrhynchus because older patterns are represented in the Oriental region within more than 100 species of lycids from several lineages. Advergence was likely the cause of the observed intraspecific polymorphism in contrast to the predicted universal monomorphism. Polymorphism was found in populations of two species in Sumatra and Borneo and in populations fine-tuned to subtle variants in various habitats. The advergence is likely to be based on the small population sizes of immigrants. The differences in population sizes result in much higher benefits for dispersing species than native populations. Speciation was trigged by the divergence in aposematic coloration, and the genetic differences accumulated slowly during incomplete isolation. We assumed that the differentiation in genitalia through sexual selection ultimately reinforced speciation initiated by the shift between mimicry patterns.     

THE DIVERSITY AND EVOLUTION OF BATESIAN MIMICRY IN PAPILIO SWALLOWTAIL BUTTERFLIES

Papilio swallowtail butterflies exhibit a remarkable diversity of Batesian mimicry, manifested in several sex-limited and polymorphic types. There is little understanding of how this diversity is distributed within Papilio , and how different mimicry types have evolved in relation to each other. To answer these questions, I present a graphical model that connects various mimicry types by hypothetical character state changes within a phylogenetic framework. A maximum likelihood analysis of evolution of mimicry types on the Papilio phylogeny showed that sexually monomorphic mimicry and female-limited mimicry have evolved repeatedly but predominantly independently in different clades. However, transitions between these mimicry types are rarely observed. The frequency distribution of character state changes was skewed in favor of the evolution of mimicry, whereas many theoretically plausible character state changes, especially evolutionary loss of mimicry, were not evident. I discuss these findings in relation to studying the tempo of evolutionary change, loss of traits, and directionality and connectivity among character states. The pathway approach and phylogenetic patterns of mimicry demonstrated in Papilio are useful to test novel hypotheses regarding the diversity and evolutionary directionality of Batesian mimicry in other systems.     

THE EVOLUTION OF DOMINANCE: A THEORY WHOSE TIME HAS PASSED?

The evolution of dominance by the selection of modifiers of the phenotypes of deleterious mutations was proposed as a hypothesis by R. A. Fisher in 1928. It has been strongly criticized ever since, is regarded by many as having been made irrelevant by metabolic control theory, and most recently has been claimed to have been‘falsified’by H. A. Orr. Is it indeed not only obsolete but wrong? Its history is reviewed and its present status evaluated. We conclude (1) that it has a role as the explanation of the dominance found in many cases of selection through visual predation and (2) that the selection mechanism long claimed to be ineffective (the increase in frequency of a single modifier) will be effective under certain special conditions that may be different from those Fisher proposed.     

EVOLUTION OF THE SOCIAL‐LEARNER‐EXPLORER STRATEGY IN AN ENVIRONMENTALLY HETEROGENEOUS TWO‐ISLAND MODEL

Social‐learner‐explorer (SE) is a learning strategy that combines accurate social learning with exploratory individual learning in that order. Arguably, it is one of the few plausible learning strategies that can support cumulative culture. We investigate numerically the factors that affect the evolution of SE in an environmentally heterogeneous two‐island model. Conditions favorable to the evolution of SE include a small exogenous cost of social learning, the occurrence of migration after social learning but before individual learning, the ability to adaptively modify the behavioral phenotype in the postmigration environment (asymmetrical individual learning), and a relatively high migration rate. The implications of our model for the evolution of SE in humans are discussed. Of particular interest is the prediction that behaviors affecting fitness would have to be socially learned in the natal environment and then subsequently modified by individual learning in the postmigration environment, suggesting a life‐cycle stage dependent reliance on the two types of learning.     

子叶节区理论与木材结构的演化

从系统发育看,出现最早的应是早已灭亡的乔木状蕨类植物的隐花植物式木材,例如：Ｌｅｐｉｄｏｄｅｎｄｒｏｎ,ｓｐｈｅｎｏｐｈｙｌｌｕｍ等。现存的都是出现在古生代末期和中生代以后的显花植物式木材,它包括裸子植的的叶子树材与被子植物的痴味树材。     

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.     

AN INTEGRATIVE TEST OF THE DEAD‐END HYPOTHESIS OF SELFING EVOLUTION IN TRITICEAE (POACEAE)

Self‐fertilization is hypothesized to be an evolutionary dead end because reversion to outcrossing can rarely happen, and selfing lineages are thought to rapidly become extinct because of limited potential for adaptation and/or accumulation of deleterious mutations. We tested these two assumptions by combining morphological characters and molecular‐evolution analyses in a tribe of hermaphroditic grasses (Triticeae). First, we determined the mating system of the 19 studied species. Then, we sequenced 27 protein‐coding loci and compared base composition and substitution patterns between selfers and outcrossers. We found that the evolution of the mating system is best described by a model including outcrossing‐to‐selfing transitions only. At the molecular level, we showed that regions of low recombination exhibit signatures of relaxed selection. However, we did not detect any evidence of accumulation of nonsynonymous substitutions in selfers compared to outcrossers. Additionally, we tested for the potential deleterious effects of GC‐biased gene conversion in outcrossing species. We found that recombination and not the mating system affected substitution patterns and base composition. We suggest that, in Triticeae, although recombination patterns have remained stable, selfing lineages are of recent origin and inbreeding may have persisted for insufficient time for differences between the two mating systems to evolve.     

从顶枝学说、中柱学说和子叶节区学说看维管植物的形态演化和起源

作者对当前植物形态学中与维管植物的形态演化和起源有着十分密切关系的顶枝学说,中柱学说与子叶节区学说进行了全面研究。并结合半个多世纪以来国际上著名的植物系统学家的维管植物分类系统,反复进行了比较和研究,对其中认为不妥之处提出了我们的见解,具体反映在文后的“维管植物系统的系统发育图”中。     

OOGAMOUS REPRODUCTION,WITH TWO‐STEP AUXOSPORULATION,IN THE CENTRIC DIATOM THALASSIOSIRA PUNCTIGERA (BACILLARIOPHYTA)1

Thalassiosira species are common components of marine planktonic communities worldwide and are used intensively as model experimental organisms. However, data on life cycles and sexuality within the genus are fragmentary. A clone of the cosmopolitan marine diatom Thalassiosira punctigera Cleve emend. Hasle was isolated from the North Sea and oogamous sexual reproduction was observed in culture. Cells approximately 45 μm and smaller became sexualized. Oogonia were produced preferentially and spermatogenesis was infrequent. Unfertilized oogonia always aborted and their development was apparently arrested at prophase of meiosis I. Further progression through meiosis and auxospore formation occurred only after a sperm had penetrated into the oocyte. Many cells of the new large‐celled generation (approximately 90–120 μm in size) immediately became sexualized again but only oogonia were produced. A few of the large oogonia became auxospores and produced initial cells 132–153 μm in diameter. The second step of auxosporulation probably involved fertilization of large‐celled oocytes by the sperm of the small‐celled spermatogonangia that were still present in the culture. An F₁ clone obtained after selfing within the small‐celled auxosporulation size range was investigated. Like the parent clone, the F₁ clone was homothallic but no auxosporulation was observed: spermatogonangia were unable to produce viable sperm, apparently because of inbreeding depression. Aggregation and interaction of oogonia were documented, and may be relevant for understanding the mechanisms of signaling and recognition between sexualized cells and the evolution of sexuality in pennate diatoms.     

GENETICS OF MIMICRY IN THE TIGER SWALLOWTAIL BUTTERFLIES,PAPILIO GLAUCUS AND P. CANADENSIS (LEPIDOPTERA: PAPILIONIDAE)

The tiger swallowtail butterfly, Papilio glaucus, exhibits a female-limited polymorphism for Batesian mimicry; the Canadian tiger swallowtail, Papilio canadensis, lacks the mimetic (dark) form entirely. The species hybridize to a limited extent where their ranges overlap. Field collections and censuses indicate that mimetic females occur throughout the range of P. glaucus but at lowest frequencies in populations at the latitudinal edges of its geographic range such as the southernmost part of Florida and along the entire northern edge of its distribution from Massachusetts to Minnesota. Frequencies of mimetic females have remained relatively stable over time. Inheritance of the mimetic form is controlled primarily by two interacting sex-linked loci. The typical matrilineal pattern of inheritance in P. glaucus can be explained by polymorphism at a Y-linked locus, b. Analysis of P. glaucus × P. canadensis crosses has also revealed an X-linked locus, s, which controls the expression of the mimetic phenotype. The P. canadensis allele, s^can, suppresses the mimetic phenotype in hybrid and backcross females. Results from more than 12 yr of rearing tiger swallowtails, including interspecies hybrids, indicate that the absence of mimetic P. canadensis females is due to both a high frequency of the “suppressing” allele s^can and low frequency of the black-pigment-determining b + allele. The frequency of s^can (or other suppressing alleles of s) in P. glaucus populations outside the hybrid zone is low. Some males heterozygous at the s locus and some suppressed mimetic females occur within the hybrid zone. A simple genetic model predicts the frequency of daughters that differ in phenotype from their mothers.     

REGULATION OF AMYLASE,CELLULASE AND CHITINASE SECRETION IN THE DIGESTIVE TRACT OF THE TWO‐SPOTTED FIELD CRICKET,Gryllus bimaculatus

The secretion of amylase and cellulase in Gryllus bimaculatus is determined by increased food intake, whereby shortly after molting food consumption increases. About half of the standing amylase concentration (activity) in the endothelial cells can be secreted within 30 min. The peak of amylase and cellulase secretion that occurs in the photophase is related to the feeding peak in the previous scotophase. The secretion of chitinase on the other hand is primarily controlled by the molting cycle. Only amylase secretion was affected by calcium in the incubation medium, suggesting an apocrine release mechanism. Refeeding experiments (after 5 days without food) suggest that the release of amylase in response to a nutrient in the lumen (glucose) is not due to simple stimulation of exocytosis, but rather a stimulation of synthesis.     

MULTIDIMENSIONAL ADAPTIVE EVOLUTION OF A FEED‐FORWARD NETWORK AND THE ILLUSION OF COMPENSATION

When multiple substitutions affect a trait in opposing ways, they are often assumed to be compensatory, not only with respect to the trait, but also with respect to fitness. This type of compensatory evolution has been suggested to underlie the evolution of protein structures and interactions, RNA secondary structures, and gene regulatory modules and networks. The possibility for compensatory evolution results from epistasis. Yet if epistasis is widespread, then it is also possible that the opposing substitutions are individually adaptive. I term this possibility an adaptive reversal. Although possible for arbitrary phenotype‐fitness mappings, it has not yet been investigated whether such epistasis is prevalent in a biologically realistic setting. I investigate a particular regulatory circuit, the type I coherent feed‐forward loop, which is ubiquitous in natural systems and is accurately described by a simple mathematical model. I show that such reversals are common during adaptive evolution, can result solely from the topology of the fitness landscape, and can occur even when adaptation follows a modest environmental change and the network was well adapted to the original environment. The possibility of adaptive reversals warrants a systems perspective when interpreting substitution patterns in gene regulatory networks.