Smith ScholarWorks Biological Sciences: Faculty Publications Biological Sciences 10-1-2014 How Discordant Morphological and Molecular Evolution Among Microorganisms Can Revise our Notions of Biodiversity on Earth Daniel J.G. Lahr Universidade de Sao Paulo - USP Haywood Dail Laughinghouse Smith College Angela M. Oliverio Smith College Feng Gao Ocean University of China Laura A. Katz Smith College, [email protected] Follow this and additional works at: https://scholarworks.smith.edu/bio_facpubs Part of the Biology Commons Recommended Citation Lahr, Daniel J.G.; Laughinghouse, Haywood Dail; Oliverio, Angela M.; Gao, Feng; and Katz, Laura A., "How Discordant Morphological and Molecular Evolution Among Microorganisms Can Revise our Notions of Biodiversity on Earth" (2014). Biological Sciences: Faculty Publications, Smith College, Northampton, MA. https://scholarworks.smith.edu/bio_facpubs/102 This Article has been accepted for inclusion in Biological Sciences: Faculty Publications by an authorized administrator of Smith ScholarWorks. For more information, please contact [email protected] NIH Public Access Author Manuscript Bioessays. Author manuscript; available in PMC 2015 October 01. NIH-PA Author ManuscriptPublished NIH-PA Author Manuscript in final edited NIH-PA Author Manuscript form as: Bioessays. 2014 October ; 36(10): 950–959. doi:10.1002/bies.201400056. How discordant morphological and molecular evolution among microorganisms can revise our notions of biodiversity on earth Daniel J. G. Lahr1, H. Dail Laughinghouse IV2, Angela Oliverio2, Feng Gao3, and Laura A. Katz2,4,* 1 Dept. of Zoology, University of Sao Paulo, Sao Paulo Brazil 2 Dept. of Biological Sciences, Smith College, Northampton, MA, USA 3 Laboratory of Protozoology, Institute of Evolution & Marine Biodiversity, Ocean University of China, Qingdao, China 4 Program in Organismal Biology and Evolution, UMass-Amherst, Amherst, MA USA Abstract Microscopy has revealed a tremendous diversity of bacterial and eukaryotic forms. More recent molecular analyses show discordance in estimates of biodiversity based on morphological analyses. Moreover, phylogenetic analyses of the diversity of microbial forms have revealed evidence of convergence at scales as large as interdomain – i.e. convergent forms shared between bacteria and eukaryotes. Here, we highlight examples of such discordance, focusing on exemplary lineages such as testate amoebae, ciliates and cyanobacteria, which have long histories of morphological study. We discuss examples in two categories: 1) morphologically identical (or highly similar) individuals that are genetically distinct and 2) morphologically distinct individuals that are genetically distinct. 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 “Thus, we have a neutral-morphology theory of evolution, where a variety of morphologies are equally successful in a particular environment. This makes an interesting contrast to the neutral-gene theory of Motoo Kimura. In the former, for one reason or another, natural selection fails to discriminate among phenotype morphologies, each of which has a distinctive genotype; in the latter, selection fails to discriminate among genotypes that all could have the same phenotype.” John Tyler Bonner, “Randomness in Evolution” *Corresponding author: Laura A. Katz [email protected]. The authors declare no conflict of interests. Lahr et al. Page 2 Introduction NIH-PA Author Manuscript NIH-PA Author ManuscriptSince NIH-PA Author Manuscript the bulk of biodiversity is microbial, and microbes play crucial roles in biogeochemical cycles and as pathogens, accurately describing the evolutionary history of microbial diversity is an important endeavor. Our understanding of microbial life on Earth has changed dramatically as microbes have been re-categorized from a single Kingdom (i.e. Protista or Protoctista) by dividing them first into bacteria (i.e. Monera) and eukaryotic microbes (i.e. Protists), and then finally into three domains with the discovery of Archaea, in 1977 (reviewed in [1]). Starting in the mid-1980s, molecular systematic studies of rDNA sequences increased our knowledge of the biodiversity of bacteria, microbial eukaryotes, and Archaea (the latter group having suffered a dearth of morphology-based studies [2]). More recently, the application of molecular techniques to analyses of whole genomes has further elucidated the tremendous diversity of microorganisms, which in turn has led to a clearer understanding of the placement of microbes across the tree of life (Fig. 1, [3, 4]). Discordance between morphology and molecules is best understood in microorganisms with a history of microscopic analyses Microscopic organisms, or “microbes”, are diverse in many aspects including morphology (the focus of this manuscript), physiology, and genetics [5]. The cannon of evolutionary biology dictates that phenotype, including morphology, reflects genotype. However, for microbes there is considerable discordance at many levels in patterns of biodiversity as assessed by morphology compared to insights from molecular data. To exemplify this discordance, we highlight examples from microbial clades that are marked by a long history of morphological study, including ciliates, testate (shelled) amoebae, and cyanobacteria. We recognize that these merely represent a ‘drop in the ocean’ of cases of discordance between morphology and molecules, and our intent here is to present key examples rather than to be exhaustive. In order to discuss the myriad of issues surrounding the discordance of morphological and molecular data at microbial levels, we consider two main types of discordance: 1) the same morphology is manifested in multiple genetic lineages (e.g. convergent morphologies, cryptic species) and 2) multiple morphologies are associated with a single genetic entity (e.g. plastic phenotypic morphologies, life cycle variants; Box 1, Fig. 2). Such categorization is helpful given the profusion of terms in the literature dealing with this complex topic [6, 7]. Hence, we opt to define the terminology used here in accordance with what seems most appropriate for microbial lineages. Our choices seek to minimize semantic discussion and focus on the biological issue. Nevertheless, it is important to remember that nature is not the least bit concerned with the categories described here, and there are surely examples of intermediary cases and/or cases that do not fit. Category 1: Cases with one morphology in multiple genetic lineages When morphologies converge Examples of convergent morphologies are common among microbial lineages, and extend from convergence between domains (e.g. eukaryotes and bacteria; Fig. 3A-F), through Bioessays. Author manuscript; available in PMC 2015 October 01. Lahr et al. Page 3 examples between major clades (Fig. 3, images G-L), to convergence at smaller levels that have led to nearly identical morphologies present among non-monophyletic lineages. At the NIH-PA Author Manuscript NIH-PA Author Manuscriptdeepest NIH-PA Author Manuscript evolutionary scales, there has been convergence to similar morphologies between lineages of bacteria and eukaryotes. For example, myxobacteria are able to produce macroscopic fruiting bodies when starved [8], hence resulting in very similar structures to those found among eukaryotic dictyostelids and myxogastrid amoebozoans (Fig. 3A-B, [9]). Similarly, the rounded aggregate morphology of small, photosynthetic organisms seems to have occurred many times in evolution, as exemplified by several cyanobacterial lineages and the volvocales (Fig. 3B-C). Finally, the microscopic hyphal form, with formation of visible colonies, has appeared independently in fungi and bacteria that absorb nutrients from their environment (Fig. 3D-E). Convergence has also occurred at deep scales within eukaryotes. For example, the shelled amoeboid body plan referred to as “testate amoebae” is present in at least two major lineages that are quite distantly related: the euglyphid testate (Fig. 3J) amoebae in the Rhizaria and the arcellinid testate amoebae (Fig. 3I) in the Amoebozoa [10]. These two lineages have traditionally been distinguished as “filose” and “lobose” testates, respectively. The tremendous genetic divergence between them has only recently been demonstrated: comprehensive multigene phylogenies indicate that the last common ancestor between these two groups is actually the last common ancestor of all eukaryotes [11, 12]. More recently, a third independent origin of shells has been revealed, as amphitremid testate amoebae (which were previously thought to be related to euglyphids) were demonstrated to be the sister group to labyrinthulids [13]. Morphological convergence between disparate groups is such a powerful deception that it has confused classification. The classical ‘Heliozoa’ (sun animalcules), characterized by a round morphology and stiff pseudopods supported by an internal bundle of microtubules, fall within four distantly-related clades in molecular analyses [14]. The strikingly similar morphology between centrohelids and actinophryids (Figures 3G and H) must be a case of convergence, because the latter are certainly stramenopile, while the former represent an orphan lineage (i.e. one without a clear sister taxon [15]). Finally, the enigmatic Stephanopogon (Fig. 3K), initially classified as a ciliate (Figure