Review
doi: 10.1101/cshperspect.a019166.Biological Scaling Problems and Solutions in Amphibians
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- PMID:26261280
- PMCID: PMC4691792
- DOI: 10.1101/cshperspect.a019166
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Review
Biological Scaling Problems and Solutions in Amphibians
Daniel L Levy et al. Cold Spring Harb Perspect Biol..
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Abstract
Size is a primary feature of biological systems that varies at many levels, from the organism to its constituent cells and subcellular structures. Amphibians populate some of the extremes in biological size and have provided insight into scaling mechanisms, upper and lower size limits, and their physiological significance. Body size variation is a widespread evolutionary tactic among amphibians, with miniaturization frequently correlating with direct development that occurs without a tadpole stage. The large genomes of salamanders lead to large cell sizes that necessitate developmental modification and morphological simplification. Amphibian extremes at the cellular level have provided insight into mechanisms that accommodate cell-size differences. Finally, how organelles scale to cell size between species and during development has been investigated at the molecular level, because subcellular scaling can be recapitulated using Xenopus in vitro systems.
Copyright © 2016 Cold Spring Harbor Laboratory Press; all rights reserved.
Figures
Changes in cell size are accompanied by modification of cell and tissue architecture. (A)Eurycea bislineata (northern two-lined salamander) larvae of differing ploidy are shown. Polyploids occur spontaneously in nature at a frequency of 5%–10% for triploids and <1% for tetraploids. With increasing ploidy, cell sizes increase and cell numbers decrease, so that, ultimately, animal size remains roughly constant. In this image, one notes fewer and larger pigment cells in the head of the tetraploid as compared with the diploid. (From Fankhauser 1939; reprinted, with permission, from Oxford University Press © 1939.) (B) Nuclei in the tetraploid epidermal cells are much larger than in the diploid, and, by inference, cell size is also greater. It is evident from the metaphase cells that chromosome number is much greater in the tetraploid. (From Fankhauser 1939; reprinted, with permission, from Oxford University Press © 1939.) (C) The pentaploidNotophthalmus viridescens (eastern newt) larva at 5.5 wk of age appears similar to the diploid, except for the altered size and number of pigment cells. Spontaneous pentaploids are found in nature at a frequency of <1%. Polyploidy can also be induced by heat treatment (Fankhauser and Watson 1942). (From Fankhauser 1945b; reprinted, with permission, from The University of Chicago Press © 1945.) (D) PolyploidNotophthalmus viridescens larvae that arose spontaneously in the laboratory were fixed, sectioned, and diagramed to show tissue morphology. Although boundaries between adjacent cells are not apparent, the spacing of nuclei approximates cell sizes and positions. Cross-sections of pronephric tubules from 35- to 40-d-old larvae are shown. Tubule sizes and wall diameters are roughly the same in all three animals despite large differences in cell size and number. Increasing ploidy necessitates more dramatic cell shape changes to maintain normal tissue morphology. At some ploidy extreme, cell size must be too large to accommodate the requisite shape changes; indeed, morphological defects become apparent in highly polyploid animals (Fankhauser 1945b). (From Fankhauser 1945a; reprinted, with permission, from Wiley-Liss, A Wiley Company © 1945.) (E) The morphology of the epithelium covering the outer half of the lens was examined for the same animals described inD. The thickness of the epithelium is the same independent of ploidy, requiring cells to take on a much more elongated and flattened morphology with increasing ploidy. In contrast to the pronephric tubules, in the lens epithelium, the shape of the nuclei must also change to maintain normal tissue thickness. (From Fankhauser 1945a; reprinted, with permission, from Wiley-Liss, A Wiley Company © 1945.) (F) Photomicrographs of erythrocytes from three species ofBatrachoseps salamanders are shown.Batrachoseps campi is a nonattenuate species and most of its erythrocytes are nucleated, whereas the other two smaller species show varying degrees of enucleation. One explanation for this adaptation in the miniaturized species is to facilitate circulation by reducing erythrocyte size. Scale bar, 40 µm (A-F). (From Mueller et al. 2008; reprinted, with permission, from Elsevier © 2008.)
Relationship between egg diameter and snout-vent length of newly transformed froglets of various species. Direct developers (purple) generally have larger eggs and smaller froglets, with egg and froglet size scaling among species. In comparison, egg and froglet size do not correlate for biphasic developers with tadpoles (green).Pipa pipa, a biphasic frog with a large egg, develops from a nonfeeding tadpole under a layer of skin on the mother’s back. Despite their size differences at metamorphosis,Rana pipiens andRana catesbeiana reach similar sizes as adults.Conraua goliath andPyxicephalus adspersus become the largest adult frogs and can exceed 25 cm in length. Embryos of the Andean marsupial tree frogGastrotheca riobambae develop in the female’s dorsal pouch. Its tailed appendage, an extension of the cloaca of males, makesAscaphus truei distinct, and improves breeding success by minimizing loss of sperm in the turbulent streams inhabited by this species. (Adapted from data in Callery 2006.)
Relationship between red blood cell size and genome size among amphibians and mammals. Diamonds show genome and erythrocyte sizes for different species of urodela (red), anura (blue), and mammals (green), using data obtained from online sources. (From Gregory et al. 2007; with permission from Oxford University Press © 2007; and Gregory 2014.) Best-fit lines for these three groups are shown. Included here are only those species for which both genome size and dry red blood cell area have been reported. Unless otherwise noted, data along the x-axis reflects diploid genome size (i.e., twice the C-value). Amphibian erythrocytes and genomes scale to significantly larger sizes than mammals, which appear to have a less steep curve. However, this may not be the best comparison because mammalian red blood cells lack nuclei. Hybridization and whole genome duplication are common in amphibians and may explain why amphibian genomes and cell sizes span a much larger size range than other animals. The circles on the plot show data from the same amphibian species with differing ploidy. In these cases, erythrocyte sizes were either reported or estimated from images in the literature (Deparis and Jaylet 1975; Deparis et al. 1975; George and Lennartz 1980; Mahony and Robinson 1980; Bogart and Licht 1986; Gregory 2001a). Interestingly, the polyploid data scale similarly to the diploid species. Among amphibians, erythrocyte size correlates with cell sizes in other tissues (Kozlowski et al. 2010), and the data plotted here are consistent with ploidy effects on cell size in other tissue types, including theRana pipiens spinal cord (Pollack and Koves 1977),X. laevis lateral line (Winklbauer and Hausen 1985), and multiple different organs in newts and salamanders (Fankhauser 1939, ,b).
Intracellular scaling inXenopus. (A) Examples ofXenopus interspecies organelle scaling are shown.X. laevis andX. tropicalis frogs and eggs differ in size. Nuclei and meiotic spindles assembled de novo in egg extracts recapitulate differences in the sizes of these two subcellular structures. Nuclei assembled in interphase egg extract were stained for the nuclear pore complex (green). (From Levy and Heald 2010; reprinted, with permission, from the authors.) Spindles assembled in meiotic egg extract were visualized for tubulin (red), DNA (blue), and katanin (green). (From Loughlin et al. 2011; adapted, with permission, from Elsevier © 2011.) (B) Examples ofXenopus developmental organelle scaling are shown. Drawings of different stageX. laevis embryos are from data in Nieuwkoop and Faber (1967). Nuclei were isolated fromXenopus embryos arrested in late interphase with cycloheximide, to ensure complete karyomere fusion in early stage embryos. Nuclei were visualized as inA. Scale bar, 20 µm. (From Levy and Heald 2010; adapted, with permission, from Elsevier © 2010.) In vitro spindles were reconstituted inX. laevis egg or embryo extracts and visualized for tubulin (red) and DNA (blue). In vivoX. laevis spindles were imaged by tubulin immunofluorescence (gray) and shows tubulin (yellow) and DNA (red) staining. (All spindle images from Wilbur and Heald 2013; adapted and made available using a Creative Commons Attribution License, except for the stage 6 in vivo spindle image from Wühr et al. 2008; adapted, with permission, from Elsevier © 2008.) Scale bar, 10 µm. (C) Scaling of spindle length by limiting cytoplasmic volume was shown using a microfluidic encapsulation technique. Cytoplasm refers toX. laevis egg extract and DNA refers to demembranatedX. laevis sperm. The boundaries of the in vitro assembled cell-like compartments consist of PEG30-PHS (polyhydroxystearate), and droplet size was tuned by varying dimensions and flow rates within the microfluidic devices. Spindles assembled in small droplets are smaller than in large droplets, mirroring spindle length scaling that occurs inX. laevis embryos during early development. Scale bar, 20 µm. (From Good et al. 2013; adapted, with permission, from the authors.) Similar results were reported in Hazel et al. (2013).
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