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Evolution of Developmental Programs in Volvox (Chlorophyta)1 J. Phycol. 46, 316–324 (2010) Ó 2010 Phycological Society of America DOI: 10.1111/j.1529-8817.2009.00803.x EVOLUTION OF DEVELOPMENTAL PROGRAMS IN VOLVOX (CHLOROPHYTA)1 Matthew D. Herron2,3 Department of Ecology and Evolutionary Biology, University of Arizona, 1041 E Lowell St, Tucson, Arizona 85721, USA Alexey G. Desnitskiy Department of Embryology, St. Petersburg State University, Universitetskaya nab. 7 ⁄ 9, St. Petersburg 199034, Russia and Richard E. Michod Department of Ecology and Evolutionary Biology, University of Arizona, 1041 E Lowell St, Tucson, Arizona 85721, USA The volvocine green algal genus Volvox includes The colonial volvocine algae include three 20 species with diverse sizes (in terms of both families of haploid, facultatively sexual eukaryotes— diameter and cell number), morphologies, and Tetrabaenaceae, Goniaceae, and Volvocaceae—in developmental programs. Two suites of characters the chlorophycean order Volvocales (Nozaki et al. are shared among distantly related lineages within 2000, Nozaki 2003a). Together with their close uni- Volvox. The traits characteristic of all species of Vol- cellular relatives in the genera Chlamydomonas and vox—large (>500) numbers of small somatic cells, Vitreochlamys, members of this group span a great much smaller numbers of reproductive cells, and diversity of morphological forms, developmental oogamy in sexual reproduction—have three or pos- programs, body sizes, and levels of complexity (Iyen- sibly four separate origins. In addition, some species gar and Desikachary 1981, Ettl 1983, Nozaki 2003b). have evolved a suite of developmental characters Unicellular forms include C. reinhardtii, an that differs from the ancestral developmental pro- important model organism for genetics, chloroplast gram. Most multicellular volvocine algae, including biogenesis, and cell-cycle regulation. The smallest some species of Volvox, share an unusual pattern of colonial forms are in the family Tetrabaenaceae cell division known as palintomy or multiple fission. (Basichlamys and Tetrabaena) and are made up of Asexual reproductive cells (gonidia) grow up to four Chlamydomonas-like cells held together in a many times their initial size and then divide several common extracellular matrix. Members of the Goni- times in rapid succession, with little or no growth aceae (Gonium and Astrephomene) range from 8 to 64 between divisions. Three separate Volvox lineages cells arranged in a flat or slightly curved plate have evolved a reduced form of palintomy in which (Gonium) or on the perimeter of a spheroid reproductive cells are small and grow between cell (Astrephomene). The diverse Volvocaceae (sensu divisions. In each case, these changes are accompa- Nozaki and Kuroiwa 1992) include seven genera nied by a reduction in the rate of cell division and (Eudorina, Pandorina, Platydorina, Pleodorina, Volvox, by a requirement of light for cell division to occur. Volvulina, and Yamagishiella) ranging from 8 to 16 Thus, two suites of characters—those characteristic cells up to 50,000 cells. Members of this family are of all Volvox species and those related to reduced mostly spheroidal (with the exception of Platydorina) palintomy—have each evolved convergently or in and may have complete, partial, or no division of parallel in lineages that diverged at least 175 million labor between reproductive and somatic cells. years ago (mya). The largest members of the Volvocaceae, in the genus Volvox, have a large number ( 500 to 50,000) Key index words: cellular differentiation; develop- of small somatic cells, which provide the flagellar ment; evolution; palintomy; Volvox action for the colony’s motility, and a few much Abbreviations: BF, Bayes factor; MCMC, Markov larger reproductive cells, or gonidia. In some cases, chain Monte Carlo; MRCA, most recent common the division of labor between somatic and reproduc- ancestor; mya, million years ago; UTEX, tive cells is complete, and reproductive cells do not University of Texas Culture Collection contribute to motility. Volvox includes at least 18 recognized species, which display a diversity of sizes, patterns of development, and details of colonial organization. The great morphological and onto- genetic diversity within this small group (Starr 1970a) led to their classification in as many as six 1Received 7 February 2009. Accepted 10 September 2009. genera in the early 20th century (Shaw 1922). These 2Author for correspondence: e-mail [email protected]. 3 genera were reduced by Printz (1927) to the rank Present address: Department of Zoology, University of British of the taxonomic sections of a single genus, Volvox. Columbia, #2370-6270 University Blvd., Vancouver, BC, Canada V6T 1Z4. 316 EVOLUTION OF DEVELOPMENT IN VOLVOX 317 Later, Smith (1944) reduced the number of sections ii, V. spermatosphaera, V. gigas, and V. pocockiae. These from six to four (see Table 1). Volvox, like several species have large gonidia, a high rate of cell divi- other nominal genera of volvocine algae, is polyphy- sion, and no determination of cell fate by means of letic (Larson et al. 1992, Coleman 1999, Nozaki unequal (asymmetric) division. Their development et al. 2000, Nozaki 2003a), but the correspondence is characterized by an unusual pattern of cell divi- between the sections and evolutionary lineages is sion known as palintomy, or rapid multiple fission. imperfect. Although a number of Volvox ontogenetic This term is sometimes used in the protistological traits have been used as taxonomic criteria (Smith literature (Sleigh 1989, Desnitski 1992, 1995) to des- 1944, Starr 1970b, Desnitskiy 1997), comparison ignate the process during which a large parental cell with molecular data shows that some such charac- undergoes a rapid sequence of repeated divisions ters have evolved convergently and are not reliable without intervening growth. Other terms have been indicators of phylogeny. used to describe cell division in the volvocine algae, Volvox, particularly V. carteri, has been developed as such as ‘‘schizogonous division’’ (Ettl 1981, 1988) a model for the developmental genetics of multicellu- and ‘‘sporulation’’ (Sluiman et al. 1989), but none larity and cellular differentiation (Kirk 1998, 2001). of these terms is as pertinent to our work as ‘‘palin- Very few recent publications have dealt with the tomy,’’ because, as we discuss below, not all species development of other representatives of this genus. of Volvox are palintomic. Kirk (2005) defined a sequence of developmental Outside of the genus Volvox, all colonial volvocine changes, most stages of which are represented in genera (e.g., Gonium, Pandorina, Eudorina, Pleodorina) extant volvocine species, that would have been are palintomic; they have large asexual reproductive required for a unicellular ancestor, presumably simi- cells, which divide rapidly and without asymmetric lar to C. reinhardtii, to evolve into a large, completely division (Coleman 1979). Therefore, all of these differentiated colony such as V. carteri. Herron and other colonial algae are characterized by the first Michod (2008) traced the evolution of these charac- developmental program. Chlamydomonas and other ters through the volvocine phylogeny and concluded closely related unicellular volvocine algae are also that some had complex histories with multiple characterized by rapid light-independent multiple fis- origins and reversals. Here we apply a similar sion (Spudich and Sager 1980). Such a palintomic approach to the evolution of developmental charac- asexual cycle closely resembles the first developmen- ters found only in the genus Volvox. tal program of Volvox (except, of course, for the Taking into account the size of mature gonidia, absence of differentiation into two cell types). the rate of their division, and specific features of The second program, characteristic of V. carteri the formation of cell lineages, four programs and V. obversus, differs from the first program in (types) of asexual development of Volvox can having an asymmetric division, which forms pre- be distinguished (Desnitski 1995). The first sumptive reproductive and somatic cells of the next developmental program is characteristic of V. powers- generation. The genetics of asymmetric division and Table 1. Volvox species included in this study. Slow division, Small gonidia, Maximum Developmental Asymmetric light-dependent growth between reported Species Section program division division divisions cell number V. africanus G. S. West Merillosphaera 2 Yes No No 6,000d V. aureus Ehrenb. Janetosphaera 4 No Yes Yes 3,200d V. barberi W. Shaw Volvox 4 No Yes Yes 47,800d V. carteri f. kawasakiensis Nozaki Merillosphaera 2 Yes No No 3,000c V. carteri f. nagariensis M. O. P. Merillosphaera 2 Yes No No 8,000a Iyengar V. carteri f. weismannia (Powers) Merillosphaera 2 Yes No No 7,500c M. O. P. Iyengar V. dissipatrix (W. Shaw) Printz Copelandosphaera 4 No Yes Yes 31,800d V. gigas Pocock Merillosphaera 1 No No No 3,000e V. globator L. Volvox 4 No Yes Yes 22,000a V. obversus (W. Shaw) Printz Merillosphaera 2 Yes No No 4,000b V. rousseletii G. S. West Volvox 4 No Yes Yes 42,000d V. tertius Meyer Merillosphaera 3 No Yes No 2,000d Sections are from Smith (1944) as modified by Kirk (1998); developmental programs are defined in Desnitski (1995). ‘‘Small goni- dia’’ refers to the size of mature asexual reproductive cells (just before the onset of cleavage). Reported cell numbers vary among authors and are intended to illustrate the overall pattern rather than to provide precise values for natural and
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