Cellular differentiation and individuality in the 'minor' multicellular taxa

Abstract

Biology needs a concept of individuality in order to distinguish organisms from parts of organisms and from groups of organisms, to count individuals and compare traits across taxa, and to distinguish growth from reproduction. Most of the proposed criteria for individuality were designed for 'unitary' or 'paradigm' organisms: contiguous, functionally and physiologically integrated, obligately sexually reproducing multicellular organisms with a germ line sequestered early in development. However, the vast majority of the diversity of life on Earth does not conform to all of these criteria. We consider the issue of individuality in the 'minor' multicellular taxa, which collectively span a large portion of the eukaryotic tree of life, reviewing their general features and focusing on a model species for each group. When the criteria designed for unitary organisms are applied to other groups, they often give conflicting answers or no answer at all to the question of whether or not a given unit is an individual. Complex life cycles, intimate bacterial symbioses, aggregative development, and strange genetic features complicate the picture. The great age of some of the groups considered shows that 'intermediate' forms, those with some but not all of the traits traditionally associated with individuality, cannot reasonably be considered ephemeral or assumed transitional. We discuss a handful of recent attempts to reconcile the many proposed criteria for individuality and to provide criteria that can be applied across all the domains of life. Finally, we argue that individuality should be defined without reference to any particular taxon and that understanding the emergence of new kinds of individuals requires recognizing individuality as a matter of degree.

Keywords: cellular differentiation; individuality; life history; major transitions; multicellularity; organisms; symbiosis.

Fig. 1

Life cycle of the Chlorophyte green alga Volvox carteri. Haploid asexual spheroids undergo asymmetric cell divisions early in development, producing small somatic cells and large reproductive cells (gonidia). Each gonidium develops into a juvenile spheroid, which is eventually released from the mother spheroid. Juveniles escape from the parental spheroid possessing all of the cells they will have as adults; continued growth occurs by increases in cell size and in the volume of extracellular matrix rather than by cell division (Starr, 1969). Spheroids that are exposed to a chemical sex inducer (S.I.) produce sexual (male or female, depending on the strain) offspring (Starr, 1970). Female spheroids appear similar to asexual spheroids, but instead of approximately 12-16 reproductive cells, they produce approximately 35-45 somewhat smaller eggs (Starr, 1969). Males are considerably smaller, up to 512 cells, with half of the cells somatic and half producing sperm packets of 64-128 biflagellate sperm (Starr, 1969). Sperm packets are released from the male spheroids, swim to female spheroids, penetrate their surface, and dissociate into individual sperm to fertilize the eggs (Starr, 1969). Fertilized eggs mature into thick-walled, desiccation-resistant, dormant spores, which germinate upon the return of optimal growth conditions (Starr, 1969). Zygote germination involves meiosis but produces only a single haploid germling, which develops into a small asexual spheroid, along with three polar bodies (Starr, 1969, 1975). Adapted from Kirk (2001), Nishii & Miller (2010).

Fig. 2

Life cycle of the Ulvophyte green alga Ulva mutabilis. Diploid zygotes formed by the fusion of gametes develop into diploid sporophytes. Sporophytes produce haploid zoospores through meiosis, and zoospores develop into haploid gametophytes, which are morphologically indistinguishable from the sporophytes. Gametophytes are of one of two genetically determined mating types and produce gametes of the same mating type. Gametes can either fuse to form a zygote that germinates into a sporophyte or settle and develop parthenogenetically (Løvlie, 1964; Fjeld, 1972; Hoxmark & Nordby, 1974). Germlings originating as unfused gametes can either develop into gametophytes or double their chromosome number and develop as sporophytes (Föyn, 1958; Fjeld, 1972). Dashed arrows indicate meiosis. Adapted from Hoxmark & Nordby (1974).

Fig. 3

Life cycle of the red alga Porphyra yezoensis. The haploid, foliose gametophyte phase begins when a diploid spore settles and attaches to the substratum before undergoing meiosis. The resulting four-celled embryos are arranged linearly, with one end attached to the substratum (Wang et al., 2009). The cells present at this phase differ in their developmental fate, with the descendants of the most basal cell or two differentiating into the holdfast and those of the other two or three cells forming the blade (Polne-Fuller & Gibor, 1984). The gametophyte produces non-motile male and female gametes as well as haploid monospores that develop into new gametophytes. Fertilization produces diploid zygotes that divide mitotically to form carpospores, which develop into microscopic, filamentous diploid sporophytes. The diploid spores produced by sporophytes can either develop into new sporophytes (monospores) or germinate meiotically to produce gametophytes (conchospores). Dashed arrow indicates meiosis. Adapted from Polne-Fuller & Gibor (1984).

Fig. 4

Life cycle of the brown alga Ectocarpus siliculosus. Filamentous diploid sporophytes produce mitospores that develop into new sporophytes and haploid meiospores that develop into gametophytes. Gametophytes produce either male or female gametes, which can fuse to produce a sporophyte or develop mitotically into a haploid parthenosporophyte. Parthenosporophytes produce mitospores that develop into new parthenosporophytes and spores that develop into gametophytes. Diploid sporophytes and parthenosporophytes are morphologically indistinguishable, but both share a branched prostrate structure absent from the gametophyte (Müller, 1967; Charrier et al., 2008). Dashed arrows indicate meiosis. Adapted from Charrier et al. (2008).

Fig. 5

Life cycle of the social amoeba Dictyostelium discoideum. Haploid unicellular amoebae emerge from spores, feed independently on bacteria in the soil and leaf litter, and reproduce by binary fission. As food supplies dwindle, multicellular development begins, with independent cells aggregating in response to secreted pulses of cyclic AMP (Kessin, 2001; Konijn et al., 1967). The aggregated cells form a mound of up to 10⁵ cells, and the aggregated cells sometimes migrate as a “slug” (Shaulsky & Kessin, 2007). Ultimately, the aggregate develops into a fruiting body, with about 20% of the cells forming the support structure (stalk) and the remainder forming a mass of spores atop the stalk. The fruiting body places the thick-walled spores in a favourable position for being dispersed by arthropods or annelids (Bonner, 2008). Once the spores encounter good conditions, unicellular haploid amoebae hatch and again begin the independent trophic phase of the asexual life cycle. Three genetically determined mating types are known (Erdos, Raper & Vogen, 1973; Bloomfield et al., 2010), and haploid amoebae of different mating types may fuse to from a diploid zygote or macrocyst (Blaskovics & Raper, 1957; Nickerson & Raper, 1973; Saga, Okada & Yanagisawa, 1983). The macrocyst attracts and cannibalizes other haploid amoebae, which contribute to the formation of a resistant cellulose wall (O'Day, 1979; Filosa & Dengler, 1972). After a period of dormancy, the macrocyst germinates meoitically to produce haploid amoebae (Filosa & Dengler, 1972; Wallace & Raper, 1979). Dashed arrow indicates meiosis. Adapted from Strassmann & Queller (2011a).

Fig. 6

Life cycle of the peritrich ciliate Zoothamnium niveum. Multicellular development begins when a haploid disperser, or telotroch, settles and attaches to a substratum and then begins to secrete a stalk (Summers, 1938b). The first cell division is asymmetric, resulting in a larger product that becomes the apical zooid and a smaller product that becomes the terminal zooid of the first branch (Fauré-Fremiet, 1930; Summers, 1938b). Each division of the apical cell produces an apical zooid and a new branch, while branches grow by continued divisions of their respective terminal zooids (Summers, 1938b). Subapical zooids cease dividing and become feeding microzooids, some of which differentiate into macrozooids and disperse as telotrochs (Summers, 1938b). Actively dividing zooids sometimes differentiate into “microgamonts,” free-swimming cells capable of conjugation, the sexual process in ciliates (Summers, 1938a,b). Gamonts swim to another colony and fuse with one of the actively dividing cells, which resumes division and normal development after a delay of several days (Summers, 1938a). Dashed arrow indicates meiosis. Some details of the Z. niveum life cycle are not available, so this account is partly based on Z. alternans, which is morphologically similar (but smaller) and closely related (Clamp & Williams, 2006). Adapted from Rinke et al. (2007).

Fig. 7

Life cycle of the sorocarp-forming ciliate Sorogena stoianovichae. Free-swimming haploid cells reproduce asexually by mitosis. Upon starvation, free-living S. stoianovitchae cells begin to aggregate beneath the surface of the water during continuous dark. Subsequently, apparently due to light stimulation, the aggregate becomes more compact and cell-to-cell adhesion occurs. Cells produce a mucoid matrix, and the aggregate begins to rise as the sheath material absorbs water and expands upwards. Cells in the fruiting body, or sorocarp, undergo encystment as sheath elongation ceases, thus completing development (Sugimoto & Endoh, 2006). No sexual cycle is known. Adapted from Sugimoto & Endoh (2008).