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Review
. 2014 Oct;36(10):950-9.
doi: 10.1002/bies.201400056. Epub 2014 Aug 25.

How discordant morphological and molecular evolution among microorganisms can revise our notions of biodiversity on Earth

Daniel J G Lahr  1 , Haywood Dail Laughinghouse 4th, Angela M Oliverio, Feng Gao, Laura A Katz
Affiliations
Review

How discordant morphological and molecular evolution among microorganisms can revise our notions of biodiversity on Earth

Daniel J G Lahr et al. Bioessays. 2014 Oct.

Abstract

Microscopy has revealed tremendous diversity of bacterial and eukaryotic forms. Recent molecular analyses show discordance in estimates of biodiversity between morphological and molecular analyses. Moreover, phylogenetic analyses of the diversity of microbial forms reveal evidence of convergence at scales as deep as interdomain: morphologies shared between bacteria and eukaryotes. Here, we highlight examples of such discordance, focusing on exemplary lineages such as testate amoebae, ciliates, and cyanobacteria. These have long histories of morphological study, enabling deeper analyses on both the molecular and morphological sides. We discuss examples in two main categories: (i) morphologically identical (or highly similar) individuals that are genetically distinct and (ii) morphologically distinct individuals that are genetically the same. We argue that hypotheses about discordance can be tested using the concept of neutral morphologies, or more broadly neutral phenotypes, as a null hypothesis.

Keywords: microbial evolution; molecular data; morphology; neutral evolution.

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Figures

Figure 1
Figure 1
A simplified tree of life, including all three major domains. Lineages in bold are discussed in this manuscript. Relationships based on [11, 80, 81].
Figure 2
Figure 2
Categories of molecular and morphological discordance among microbes from a phylogenetic perspective. To the left, one morphology, multiple lineages category. To the right, one lineage, multiple morphologies.
Figure 3
Figure 3
Examples of striking morphological convergence between bacterial and eukaryotic domains (A-F) and among deeply-diverged eukaryotic clades (G-L). A: Fruiting bodies of Trichia varia, an amoebozoan eukaryote. B: Fruiting bodies of Myxococcus xanthus, a bacterium. C: Gloeocapsa sp., a cyanobacterium. D: Pandorina morum, a green alga. E: a colony of the bacterium Streptomyces. F: a colony of the fungus Penicillium. The last common ancestor between the organisms in figure A and B, C and D, and E and F is the last common ancestor of all life, thus, each of these pairs of organisms must have diverged over 3.5 billion years ago; G: Acanthocystis penardi, the “sun-animalcule”, a centrohelid eukaryote (group with unknown affinities). H: Actinosphaerium eichorni, another “sun-animalcules”, however, molecular data has shown that this is a stramenopile (related to diatoms). I: Quadrullela, an arcellinid amoebozoan, or lobose testate amoeba. J: Euglypha, and euglyphid rhizarian, or filose testate amoeba. K: Stephanopogon apogon, a heterolobosean, the heterolobosea are typically characterized by amoeboid forms with a flagellate life-cycle stage. L: Spathidium, a ciliate. In these eukaryotic pairs of organisms, each of the pair belongs in a very distant clade to the other, with a last common ancestor only billions of years ago. Image credits: B, E, F are from Wikimedia; A, C, D, J are from micro*scope; G, H were kindly provided by Mr. Wolfgang Bettighoefer; J is from Daniel Lahr.
Figure 4
Figure 4
Historical reconstruction of relationships and morphology of nebelids. A: Phylogenetic history of nebelids, based on SSU rDNA. Drawings represent morphologies. The red branches in tree highlight instances where identical SSU rDNA sequences exist for both Hyalosphenia papilio and Hyalosphenia elegans. B: Light microscope images of H. elegans, and C: of H. papilio showing highly distinct morphologies. Images B and C are to the same scale, scale bar is 30 μm. Phylogenetic tree is based on previous studies [19, 20, 82].
Figure 5
Figure 5
Ratio of papers published proposing cryptic microbial species over total number of described microbial species from 1989-2013. Numbers of published papers were obtained by searching the online database SCOPUS with the query [species AND cryptic AND microb*]. Number of described species per year of microorganisms was obtained at the Index of Organismal Names database.
Figure 6
Figure 6
Examples of microbial morphologies interpreted according to phylogenetic contexts. A: Cryptic speciation among Phormidium cyanobacteria. Historical reconstruction based on [47]. B: Phenotypic plasticity among dinoflagellates. The dinoflagellates Ceratocorys horrida and Tripos ranipes (= Neoceratium ranipes) display intense morphological modification on a short time span. Phylogenetic framework derived from Gomez et al. [83].
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