DOCSLIB.ORG

Cellular Asymmetry in Chlamydomonas Reinhardtii

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Cellular Asymmetry in Chlamydomonas Reinhardtii Cellular asymmetry in Chlamydomonas reinhardtii JEFFREY A. HOLMES and SUSAN K. DUTCHER* Department of Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, Colorado 80309-0347, USA •Author for correspondence Summary Although largely bilaterally symmetric, the two asymmetric. As a result of asymmetric, but differ- sides of the unicellular alga Chlamydomonas rein- ent, locations of the plus and minus mating struc- hardtii can be distinguished by the location of the tures, mating preferentially results in quadriflagel- single eyespot. When viewed from the anterior end, late dikaryons with parallel flagellar pairs and both the eyespot is always closer to one flagellum than eyespots on the same side of the cell. This asymmet- the other, and located at an angle of approximately ric fusion, as well as all the other asymmetries 45° clockwise of the flagellar plane. This location described, may be necessary for the proper photo- correlates with the position of one of four acetylated tactic behavior of these cells. The invariant handed- microtubule bundles connected to the flagellar ap- ness of the spindle pole, eyespot position, and paratus. Each basal body is attached to two of these mating structure position appears to be based on microtubule rootlets. The rootlet that positions the the inherent asymmetry of the basal body pair, eyespot is always attached to the same basal body, providing an example of how an intracellular pat- which is the daugher of the parental/daughter basal tern can be determined and maintained. body pair. At mitosis, the replicated basal body pairs segregate in a precise orientation that main- tains the asymmetry of the cell and results in mitotic poles that have an invariant handedness. Key words: Chlamydomonas, asymmetry, basal bodies, The fusion of gametic cells during mating is also acetylated tubulin, eyespot, uni mutants. Introduction Using the eyespot as a marker, it has been shown that the flagellar apparatus has a physiological cis/trans The number and position of organelles within a cell of asymmetry. Kamiya and Witman (1984) have shown that Chlamydomonas is highly stereotyped. Most of the or- reactivated cis and trans axonemes have different and ganelles are symmetrically positioned around the long opposite responses to calcium concentration, and Huang axis of the cell (Fig. 1). The most striking exception to et al. (1982) have described a number of mutations (the this rotational symmetry is the position of the eyespot, a uni mutants) whose defect appears to be at the level of the red-pigmented structure that acts as an antenna for the basal body and whose distinguishing feature is that they photoreceptor in the plasma membrane above it (Foster fail to assemble the cis flagellum, but remain able to and Smyth, 1980). Each cell normally contains a single assemble the trans flagellum. Clearly the cis and trans eyespot, which is always located at the periphery of the basal bodies and axonemes are not equivalent. cell, in a location closer to one flagellum than the other. The basal bodies of Chlamydomovas replicate and The asymmetric position of the eyespot can be used to segregate in a manner similar to that of mammalian differentiate the cell into two halves. By convention, the centrioles. During mitotic prophase in Chlamydomonas half of the cell containing the eyespot is denoted cis, and the two probasal bodies extend to full length and are the other half trans (Huang et al. 1982). An imaginary segregated in a semiconservative manner, so that one cis/trans plane that passes between the two basal bodies parental and one daughter basal body go to each mitotic can be used to differentiate these two halves. To aid in pole (Gaffel, 1988). The parental/daughter difference in description, we have added the terms syn and and to the two basal bodies is postulated to be the source of the describe the two halves of the cell differentiated by a physiological difference between the two basal bodies and second imaginary plane in which the two flagella beat. the basis of the Uni~ phenotype (Huang et al. 1982). This is commonly referred to as the flagellar plane. The Chlamydomonas is not unique in having two different locations of these two planes of reference are shown flagella, and in fact no example of truly identical flagella diagrammatically in Fig. 2. on a biflagellate algal cell has yet been reported. In several Journal of Cell Science 94, 273-285 (1989) Printed in Great Britain © The Company of Biologists Limited 1989 273 algal species it has now been shown that the differences between the flagella correlate with the parental/daughter history of the two basal bodies (Beech et al. 1980; Melkonian et al. 1987; Wetherbeee^a/. 1988). Because of this we believe the correct positioning of the eyespot occurs with respect to an inherently asymmetric parental/ daughter basal body pair. The position of the eyespot is believed to be deter- mined by a unique bundle of microtubules attached to the flagellar apparatus (Melkonian, 1984a; Moestrup, 1978). Each of the two basal bodies has two cytoplasmic microtubule roots or rootlets attached to it (Ringo, 1967). These rootlets differ from one another both in the number of microtubules they contain and in their angular position with respect to the flagellar plane. The four- membered microtubule rootlets extend at an angle of approximately 45° clockwise of the flagellar plane (all clockface distinctions are made from a point of reference outside the cell, facing the cell's anterior end) and the two-membered rootlets extend at an approximately 45° counterclockwise angle. The hypothesis that the eyespot is positioned by a rootlet is supported by the coincidence of the eyespot position and the angular position of the four-membered rootlet, as well as by the observation of a Fig. 1. Schematic diagram of the flagellar apparatus of band of microtubules seen in association with the eyespot Chlamydomonas reinhardtii. The view is from the anterior in electron micrographs (Gruber and Rosario, 1974). In end of the cell and demonstrates the 180° rotational other green algae, the eyespot is always found associated symmetry of the flagellar apparatus, bb. The two mature with the microtubule rootlet that corresponds, both in basal bodies, pbb. The probasal bodies that assemble the microtubule number and position, to the four-membered daughter basal bodies prior to mitosis. Their connections to rootlet of Chlamydomonas (Moestrup, 1978). the flagellar apparatus are omitted, df. The distal striated fiber that connects the basal bodies. Two smaller proximal Presumably the angular position of the rootlets is striated fibers are mostly obscured in this diagram. determined by a specific site of attachment for each cv. Contractile vacuoles whose location is represented by the rootlet type to each basal body. Chlamydomonas basal broken circles. Two types of microtubule rootlets emanate bodies are not rotationally symmetric and each micro- from the flagellar apparatus, composed of two and four tubule triplet can be numbered around the basal body microtubules, respectively, sf. Striated fibers associated with cylinder (Hoops and Witman, 1983). Examination of a both rootlet types. All four microtubule rootlets terminate in Chlamydomonas mutant (vfi-3) in which the fibers con- the region beneath the distal fiber, although the striated necting basal bodies are incomplete (Hoops et al. 1984; component of the two-membered rootlets is continuous. Wright et al. 1983) as well as observations of other green algae, which undergo a rotation of their basal bodies during development (Greuel and Floyd, 1985; Hoops, cis trans 1984; Taylor et al. 1985), support the idea that the rootlets and other components of the flagellar apparatus are physically connected to the basal bodies at unique sites. syn The position of the eyespot not only makes cells of Chlamydomonas asymmetric, but enantiomeric as well. That is, they exist in only one mirror-image configur- ation. When viewed from the anterior end, the eyespot is always located at an angle of approximately 45° from the plane determined by the two flagella (Fig. 2). Only the enantiomorph in which the eyespot is clockwise of the I flagellar plane exists in nature (Ruffer and Nultch, 1985); the counterclockwise enantiomorph has not been ob- Fig. 2. Diagram of the eyespot position in an anterior view. served. This handedness of the cell is distinct from Two imaginary planes bisecting the cell are used for reference. The as/trans plane divides the cell between the cis/trans asymmetry, since it is an asymmetry within the two basal bodies. The syn/anti plane, or flagellar plane, cis half of the cell itself. contains the two basal bodies and the two flagella. The Like the cells of Chlamydomonas, basal bodies exist in eyespot is always located at an angular position of 45 ° only one enantiomeric configuration. When viewed from clockwise of the syn/anti plane, coincident with the meridian the anterior end, the microtubule triplets overlap in a containing the four-membered microtubule rootlets. clockwise direction (Fulton, 1971; Melkonian, 1984a). 274 J. A. Holmes and S. K. Dutcher Basal bodies or centrioles of the opposite handedness, 1:100; 6-11B-1 was diluted 1:10. Chlamydomonas cells were 6 7 1 where the overlap is in a counterclockwise direction, have grown in liquid to a density of approximately 10 -10 cells ml" not been observed in any organism to our knowledge. and pelleted in a clinical centrifuge. The cells were resuspended The enantiomeric position of the eyespot in the cell is in an equivalent volume of a buffer containing 30 mM-Pipes, 25mM-KCl, SmM-MgSO , 5mM-EGTA, and 12% hexylene thus believed to be a reflection of the fact that each basal 4 glycol (pH 6.8) for about 1 min and then repelleted. They were body has only one attachment site for the four-membered then lysed in 0.5 % saponin (Sigma) in the same buffer for rootlet and basal bodies exist in only one enantiomeric 1-2 min, pelleted, and fixed by the addition of 100—200/il of a form.
Load more

Recommended publications
  • Conceptual Barriers to Progress Within Evolutionary Biology
    Found Sci (2009) 14:195–216 DOI 10.1007/s10699-008-9153-8 Conceptual Barriers to Progress Within Evolutionary Biology Kevin N. Laland · John Odling-Smee · Marcus W. Feldman · Jeremy Kendal Published online: 26 November 2008 © Springer Science+Business Media B.V. 2008 Abstract In spite of its success, Neo-Darwinism is faced with major conceptual barriers to further progress, deriving directly from its metaphysical foundations. Most importantly, neo- Darwinism fails to recognize a fundamental cause of evolutionary change, “niche construc- tion”. This failure restricts the generality of evolutionary theory, and introduces inaccuracies. It also hinders the integration of evolutionary biology with neighbouring disciplines, includ- ing ecosystem ecology, developmental biology, and the human sciences. Ecology is forced to become a divided discipline, developmental biology is stubbornly difficult to reconcile with evolutionary theory, and the majority of biologists and social scientists are still unhappy with evolutionary accounts of human behaviour. The incorporation of niche construction as both a cause and a product of evolution removes these disciplinary boundaries while greatly generalizing the explanatory power of evolutionary theory. Keywords Niche construction · Evolutionary biology · Ecological inheritance · Ecosystem ecology · Developmental biology 1 Introduction On the face of it, evolutionary biology is a thriving discipline: It is built on the solid theoret- ical foundations of mathematical population biology; it has a rich and productive empirical K. N. Laland (B) School of Biology, University of St. Andrews, Bute Building, Queens Terrace, St. Andrews, Fife KY16 9TS, UK e-mail: [email protected] J. Odling-Smee Mansfield College, University of Oxford, Oxford OX1 3TF, UK M.
    [Show full text]
  • Wingless Is a Positive Regulator of Eyespot Color Patterns in Bicyclus Anynana Butterflies
    bioRxiv preprint doi: https://doi.org/10.1101/154500; this version posted June 23, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. wingless is a positive regulator of eyespot color patterns in Bicyclus anynana butterflies 1,* 1 2 1 1,3,* Nesibe Özsu , Qian Yi Chan , Bin Chen , Mainak Das Gupta , and Antónia Monteiro 1 Biological Sciences, National University of Singapore, Singapore 117543; 2 Institute of Entomology and Molecular Biology, Chongqing Normal University, Shapingba, 400047 Chongqing, China 3 Yale-NUS College, Singapore 138614 * Corresponding authors: Nesibe Özsu5or Antónia Monteiro Department of Biological Sciences, 14 Science Drive 4 Singapore, 117543 Tel: +65 97551591 [email protected] or [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/154500; this version posted June 23, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Summary 2 Eyespot patterns of nymphalid butterflies are an example of a novel trait yet, the 3 developmental origin of eyespots is still not well understood. Several genes have been 4 associated with eyespot development but few have been tested for function. One of these 5 genes is the signaling ligand, wingless, which is expressed in the eyespot centers during early 6 pupation and may function in eyespot signaling and color ring differentiation. Here we 7 tested the function of wingless in wing and eyespot development by down-regulating it in 8 transgenic Bicyclus anynana butterflies via RNAi driven by an inducible heat-shock promoter.
    [Show full text]
  • Development, Plasticity and Evolution of Butterfly Eyespot Patterns" (1996), by Paul M
    Published on The Embryo Project Encyclopedia (https://embryo.asu.edu) "Development, Plasticity and Evolution of Butterfly Eyespot Patterns" (1996), by Paul M. Brakefield et al. [1] By: Zou, Yawen Keywords: Butterfly eyespots [2] Paul M. Brakefield experiment [3] Bush-brown butterfly [4] eyespot patterns [5] Paul M. Brakefield and his research team in Leiden, the Netherlands, examined the development, plasticity, ande volution [6] of butterfly [7] eyespot patterns, and published their findings in Nature in 1996. Eyespots are eye-shaped color patterns that appear on the wings of some butterflies and birds [8] as well as on the skin of some fish [9] and reptiles. In butterflies, such as the peacock butterfly [7] (Aglais io [10]), the eyespots resemble the eyes of birds [8] and help butterflies deter potential predators. Brakefield's research team described the stages through which eyespots develop, identified the genes [11] and environmental signals that affect eye-spot appearance in some species, and demonstrated that small genetic variations can change butterfly [7] eyespot color and shape. The research focused on a few butterfly [7] species, but it contributed to more general claims of how the environment may affect the development of coloration and how specific color patterns may have evolved. At the time of experiment, Brakefield was a Chair in Evolutionary Biology at the University of Leiden [12], in Leiden, the Netherlands, though in 2010 he moved to Cambridge, UK to direct the University Museum of Zoology. While in Leiden, he persued a research program in evolutionary developmental biology [13] and had started working on butterfly [7] eyespots in collaboration with Vernon French, who was at the University of Edinburgh [14] in Edinburgh, Scotland.
    [Show full text]
  • Temporal Flexibility of Gene Regulatory Network Underlies a Novel Wing Pattern in Flies
    Temporal flexibility of gene regulatory network underlies a novel wing pattern in flies Héloïse D. Dufoura,b, Shigeyuki Koshikawa (越川滋行)a,b,1,2,3, and Cédric Fineta,b,3,4 aHoward Hughes Medical Institute, University of Wisconsin, Madison, WI 53706; and bLaboratory of Molecular Biology, University of Wisconsin, Madison, WI 53706 Edited by Denis Duboule, University of Geneva, Geneva 4, Switzerland, and approved April 6, 2020 (received for review February 3, 2020) Organisms have evolved endless morphological, physiological, and Nevertheless, it does not explain how the new expression of behavioral novel traits during the course of evolution. Novel traits the coopted toolkit genes does not interfere with the develop- were proposed to evolve mainly by orchestration of preexisting ment of the tissue. Some authors have suggested that the reuse genes. Over the past two decades, biologists have shown that of toolkit genes might only happen during late development after cooption of gene regulatory networks (GRNs) indeed underlies completion of the early function of the redeployed genes (21, 22, numerous evolutionary novelties. However, very little is known 29). However, little is known about the properties of a GRN that about the actual GRN properties that allow such redeployment. allow the cooption of one or several of its components/genes Here we have investigated the generation and evolution of the without impairing the development of the tissue. complex wing pattern of the fly Samoaia leonensis. We show that In this study, we use the complex wing pigmentation pattern of the transcription factor Engrailed is recruited independently from the fly species Samoaia leonensis as a model to address how the the other players of the anterior–posterior specification network to generate a new wing pattern.
    [Show full text]
  • Wonderful Wacky Water Critters
    Wonderful, Wacky, Water Critters WONDERFUL WACKY WATER CRITTERS HOW TO USE THIS BOOK 1. The “KEY TO MACROINVERTEBRATE LIFE IN THE RIVER” or “KEY TO LIFE IN THE POND” identification sheets will help you ‘unlock’ the name of your animal. 2. Look up the animal’s name in the index in the back of this book and turn to the appropriate page. 3. Try to find out: a. What your animal eats. b. What tools it has to get food. c. How it is adapted to the water current or how it gets oxygen. d. How it protects itself. 4. Draw your animal’s adaptations in the circles on your adaptation worksheet on the following page. GWQ023 Wonderful Wacky Water Critters DNR: WT-513-98 This publication is available from county UW-Extension offices or from Extension Publications, 45 N. Charter St., Madison, WI 53715. (608) 262-3346, or toll-free 877-947-7827 Lead author: Suzanne Wade, University of Wisconsin–Extension Contributing scientists: Phil Emmling, Stan Nichols, Kris Stepenuck (University of Wisconsin–Extension) and Mike Miller, Mike Sorge (Wisconsin Department of Natural Resources) Adapted with permission from a booklet originally published by Riveredge Nature Center, Newburg, WI, Phone 414/675-6888 Printed on Recycled Paper Illustrations by Carolyn Pochert and Lynne Bergschultz Page 1 CRITTER ADAPTATION CHART How does it get its food? How does it get away What is its food? from enemies? Draw your “critter” here NAME OF “CRITTER” How does it get oxygen? Other unique adaptations. Page 2 TWO COMMON LIFE CYCLES: WHICH METHOD OF GROWING UP DOES YOUR ANIMAL HAVE? egg larva adult larva - older (mayfly) WITHOUT A PUPAL STAGE? THESE ANIMALS GROW GRADUALLY, CHANGING ONLY SLIGHTLY AS THEY GROW UP.
    [Show full text]
  • Duke University Dissertation Template
    Evolutionary trends in phenotypic elements of seasonal forms of the tribe Junoniini (Lepidoptera: Nymphalidae) by Jameson Wells Clarke Department of Biology Duke University Date:_______________________ Approved: ___________________________ H. Fred Nijhout, Ph.D., Supervisor ___________________________ V. Louise Roth, Ph.D. ___________________________ Sonke Johnsen, Ph.D. Thesis submitted in partial fulfillment of the requirements for the degree of Master of Science in the Department of Biology in the Graduate School of Duke University 2017 i v ABSTRACT Evolutionary trends in phenotypic elements of seasonal forms of the tribe Junoniini (Lepidoptera: Nymphalidae) by Jameson Wells Clarke Department of Biology Duke University Date:_______________________ Approved: ___________________________ H. Fred Nijhout, Ph.D., Supervisor ___________________________ V. Louise Roth, Ph.D. ___________________________ Sonke Johnsen, Ph.D. An abstract of a thesis submitted in partial fulfillment of the requirements for the degree of Master of Science in the Department of Biology in the Graduate School of Duke University 2017 Copyright by Jameson Wells Clarke 2017 Abstract Seasonal polyphenism in insects is the phenomenon whereby multiple phenotypes can arise from a single genotype depending on environmental conditions during development. Many butterflies have multiple generations per year, and environmentally induced variation in wing color pattern phenotype allows them to develop adaptations to the specific season in which the adults live. Elements of butterfly
    [Show full text]
  • Origin of the Mechanism of Phenotypic Plasticity in Satyrid Butterfly Eyespots
    SHORT REPORT Origin of the mechanism of phenotypic plasticity in satyrid butterfly eyespots Shivam Bhardwaj1†*, Lim Si-Hui Jolander2, Markus R Wenk1,2, Jeffrey C Oliver3, H Frederik Nijhout4, Antonia Monteiro1,5* 1Department of Biological Sciences, National University of Singapore, Singapore, Singapore; 2Department of Biochemistry, National University of Singapore, Singapore, Singapore; 3Office of Digital Innovation & Stewardship, University of Arizona, Tucson, United States; 4Department of Biology, Duke University, Durham, United States; 5Yale-NUS College, Singapore, Singapore Abstract Plasticity is often regarded as a derived adaptation to help organisms survive in variable but predictable environments, however, we currently lack a rigorous, mechanistic examination of how plasticity evolves in a large comparative framework. Here, we show that phenotypic plasticity in eyespot size in response to environmental temperature observed in Bicyclus anynana satyrid butterflies is a complex derived adaptation of this lineage. By reconstructing the evolution of known physiological and molecular components of eyespot size plasticity in a comparative framework, we showed that 20E titer plasticity in response to temperature is a pre-adaptation shared by all butterfly species examined, whereas expression of EcR in eyespot centers, and eyespot sensitivity to 20E, are both derived traits found only in a *For correspondence: subset of species with eyespots. [email protected] (SB); [email protected] (AM) Introduction Present address: †Department
    [Show full text]
  • The Genetic Basis of Hindwing Eyespot Number Variation in Bicyclus
    bioRxiv preprint doi: https://doi.org/10.1101/504506; this version posted December 21, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 The genetic basis of hindwing eyespot number variation in Bicyclus 2 anynana butterflies 3 4 Angel G. Rivera-Colón*, †, Erica L. Westerman‡, Steven M. Van Belleghem†, Antónia 5 Monteiro§,**, and Riccardo Papa† 6 7 Affiliations 8 *Department of Animal Biology, University of Illinois, Urbana-Champaign 9 †University of Puerto Rico-Rio Piedras Campus 10 ‡University of Arkansas, Fayetteville 11 §National University of Singapore 12 **Yale-NUS College 13 14 Data accessibility 15 The Bicyclus anynana PstI RAD-tag sequencing data is available via the Genbank 16 Bioproject PRJNA509697. Genotype VCF files will be made available through figshare 17 upon acceptance. 1 bioRxiv preprint doi: https://doi.org/10.1101/504506; this version posted December 21, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 18 Running Title: Genetics of eyespot number variation 19 20 Key words: Serial homology, genetics, apterous, eyespot number, Bicyclus anynana, 21 genetic architecture 22 23 Co-Corresponding Authors: 24 [email protected] and [email protected] 2 bioRxiv preprint doi: https://doi.org/10.1101/504506; this version posted December 21, 2018.
    [Show full text]
  • Eyespot-Assembly Mutants in Chlamydomonas Reinhardtii
    Copyright 1999 by the Genetics Society of America Eyespot-Assembly Mutants in Chlamydomonas reinhardtii Mary Rose Lamb,* Susan K. Dutcher,² Cathy K. Worley³ and Carol L. Dieckmann³ *Department of Biology, University of Puget Sound, Tacoma, Washington 98416-0320, ²Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder, Colorado 80309 and ³Department of Biochemistry, University of Arizona, Tucson, Arizona 85721 Manuscript received April 28, 1999 Accepted for publication June 25, 1999 ABSTRACT Chlamydomonas reinhardtii is a single-celled green alga that phototaxes toward light by means of a light- sensitive organelle, the eyespot. The eyespot is composed of photoreceptor and Ca11-channel signal transduction components in the plasma membrane of the cell and re¯ective carotenoid pigment layers in an underlying region of the large chloroplast. To identify components important for the positioning and assembly of a functional eyespot, a large collection of nonphototactic mutants was screened for those with aberrant pigment spots. Four loci were identi®ed. eye2 and eye3 mutants have no pigmented eyespots. min1 mutants have smaller than wild-type eyespots. mlt1(ptx4) mutants have multiple eyespots. The MIN1, MLT1(PTX4), and EYE2 loci are closely linked to each other; EYE3 is unlinked to the other three loci. The eye2 and eye3 mutants are epistatic to min1 and mlt1 mutations; all double mutants are eyeless. min1 mlt1 double mutants have a synthetic phenotype; they are eyeless or have very small, misplaced eyespots. Ultrastructural studies revealed that the min1 mutants are defective in the physical connection between the plasma membrane and the chloroplast envelope membranes in the region of the pigment granules.
    [Show full text]
  • Hedgehog Signaling Enables Nutrition-Responsive Inhibition of an Alternative Morph in a Polyphenic Beetle
    Hedgehog signaling enables nutrition-responsive inhibition of an alternative morph in a polyphenic beetle Teiya Kijimotoa,b,1 and Armin P. Moczeka aDepartment of Biology, Indiana University, Bloomington, IN 47405; and bDivision of Plant and Soil Sciences, West Virginia University, Morgantown, WV 26506 Edited by David L. Denlinger, Ohio State University, Columbus, OH, and approved April 4, 2016 (received for review February 3, 2016) The recruitment of modular developmental genetic components development of two or more discrete morphs or castes—has be- into new developmental contexts has been proposed as a central come increasingly recognized for its importance as a potential mechanism enabling the origin of novel traits and trait functions facilitator of adaptive radiations (8). For instance, in many butterfly without necessitating the origin of novel pathways. Here, we in- species, seasonal conditions critically alter selective environments, vestigate the function of the hedgehog (Hh) signaling pathway, a and seasonal sensitivity in eye spot formation is able to adjust wing highly conserved pathway best understood for its role in patterning phenotypes, thereby maintaining high fitness across fluctuating anterior/posterior (A/P) polarity of diverse traits, in the develop- environments (9). Similarly, environment-dependent induction mental evolution of beetle horns, an evolutionary novelty, and horn of carnivory in spadefoot toad tadpoles (10, 11) or tooth for- polyphenisms, a highly derived form of environment-responsive mation and bacterial predation in nematodes (12), two striking trait induction. We show that interactions among pathway members and complex evolutionary novelties, greatly affect the adaptive are conserved during development of Onthophagus horned beetles significance of each innovation, thereby facilitating their adaptive and have retained the ability to regulate A/P polarity in traditional radiations (13).
    [Show full text]
  • 11 Endocrine Control of Insect Polyphenism
    11 Endocrine Control of Insect Polyphenism K. Hartfelder Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil D.J. Emlen University of Montana, Missoula, MT, USA © 2012 Elsevier B.V. All Rights Reserved Summary the insulin-signaling pathway is now also emerging as a Polyphenism in insects is associated with some of the major player. We present an overview of current knowl- most striking and successful life histories. Insect poly- edge regarding wing length dimorphism in crickets, phenisms center around four major themes: wing the gradual phase shift from the solitary to gregarious length variation (including winglessness), differences syndrome in migrating locusts, the complex switch- in fertility or reproductive strategies, body and/or wing ing between wingless/winged forms and asexual/sexual coloration and exaggerated morphologies. Hormones, reproduction in aphids, wing and body color variants in especially juvenile hormone and ecdy steroids are butterflies, male horn dimorphism in beetles, and caste important factors underlying the generation of dis- polyphenism occurring in the hemimetabolous termites tinct morphologies and reproductive strategies, and and holometabolous hymenopterans. 11.1. Polyphenism and Polymorphism: Discontinuity in the Variation of Insects 464 11.2. Polyphenism in the Hemimetabola 465 11.2.1. Hemiptera/Homoptera Wing Polyphenism 465 11.2.2. Orthoptera 470 11.2.3. “Isoptera” (Termites) — Caste Polyphenism in the Hemimetabola 476 11.3. Polyphenism in the Holometabola 479 11.3.1. Lepidoptera 479 11.3.2. Coleoptera — Male Dimorphism for Weaponry 484 11.3.3. Hymenoptera — Caste Polyphenism and Division of Labor 487 11.4. Synthesis and Perspectives 501 11.1. Polyphenism and Polymorphism: Discontinuity in the Variation of Insects focus on relatively discrete or discontinuous variation in Historically, the terms polymorphism and polyphen- phenotype expression.
    [Show full text]
  • Macroevolutionary Shifts of Wnta Function Potentiate Butterfly Wing-Pattern Diversity
    Macroevolutionary shifts of WntA function potentiate butterfly wing-pattern diversity Anyi Mazo-Vargasa, Carolina Conchab,1, Luca Livraghic,1, Darli Massardod,1, Richard W. R. Wallbankb,e,1, Linlin Zhanga, Joseph D. Papadorf, Daniel Martinez-Najeraf, Chris D. Jigginsb,e, Marcus R. Kronforstd, Casper J. Breukerc, Robert D. Reeda, Nipam H. Patelf,g, W. Owen McMillanb, and Arnaud Martinh,2 aDepartment of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853; bSmithsonian Tropical Research Institute, Gamboa, Panama; cDepartment of Biological and Medical Sciences, Oxford Brookes University, Oxford OX3 0BP, United Kingdom; dDepartment of Ecology and Evolution, University of Chicago, Chicago, IL 60637; eDepartment of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom; fDepartment of Integrative Biology, University of California, Berkeley, CA 94720; gDepartment of Molecular Cell Biology, University of California, Berkeley, CA 94720; and hDepartment of Biological Sciences, The George Washington University, Washington, DC 20052 Edited by Sean B. Carroll, Howard Hughes Medical Institute and University of Wisconsin–Madison, Madison, WI, and approved August 7, 2017 (received for review May 16, 2017) Butterfly wing patterns provide a rich comparative framework to framework, patterns are organized into parallel subdivisions of study how morphological complexity develops and evolves. Here autonomous color pattern complexes known as “symmetry sys- we used CRISPR/Cas9 somatic mutagenesis to test a patterning tems,” which are arranged across the dorsal and ventral surfaces of role for WntA, a signaling ligand gene previously identified as a both the fore- and hindwing (14–19) (Fig. 1 A–C). This arrange- hotspot of shape-tuning alleles involved in wing mimicry.
    [Show full text]