Genome Size Covaries More Positively with Propagule Size than Adult Size: New Insights into an Old Problem

Abstract

The body size and (or) complexity of organisms is not uniformly related to the amount of genetic material (DNA) contained in each of their cell nuclei ('genome size'). This surprising mismatch between the physical structure of organisms and their underlying genetic information appears to relate to variable accumulation of repetitive DNA sequences, but why this variation has evolved is little understood. Here, I show that genome size correlates more positively with egg size than adult size in crustaceans. I explain this and comparable patterns observed in other kinds of animals and plants as resulting from genome size relating strongly to cell size in most organisms, which should also apply to single-celled eggs and other reproductive propagules with relatively few cells that are pivotal first steps in their lives. However, since body size results from growth in cell size or number or both, it relates to genome size in diverse ways. Relationships between genome size and body size should be especially weak in large organisms whose size relates more to cell multiplication than to cell enlargement, as is generally observed. The ubiquitous single-cell 'bottleneck' of life cycles may affect both genome size and composition, and via both informational (genotypic) and non-informational (nucleotypic) effects, many other properties of multicellular organisms (e.g., rates of growth and metabolism) that have both theoretical and practical significance.

Keywords: Crustacea; allometric scaling; cell size; cellular (nuclear) DNA content; egg and sperm sizes; life cycles; multicellular animals and plants; nucleotypic effects; spore, pollen and seed sizes; unicellular organisms.

Figure 1

Log-linear relationships between genome size (pg) and body length (mm) (A: data from [57]), wet egg mass (mg) and wet adult (maternal) body mass (mg) (B: data from [101]), genome size and wet body mass (C: data from [101,102]), and genome size and wet egg mass (D: data from [101,102]) for four major crustacean taxa. Solid and dashed lines indicate significant and non-significant linear regressions, respectively (details in Table 2).

Figure 2

Curvilinear relationships between crustacean genome size (pg) and body length (mm) (A), wet egg mass (mg) and wet adult (maternal) body mass (mg) (B), and genome size and wet body mass (C). Note contrast with linear relationship between genome size and wet egg mass (D). All relationships based on log-transformed data in Figure 1 (statistical details in Table 4).

Figure 3

Schematic diagrams illustrating relationships between genome size, cell size and body size in unicellular and multicellular organisms, following predictions #2 and #3 of the Single-Cell ‘Bottleneck’ Hypothesis (SCBH: Table 6). (A): Genome size (indicated by the size of the black nucleus in each cell) correlates positively with cell size in unicellular organisms. (B): Genome size correlates positively with body size in multicellular organisms that differ largely in cell size. (C): Genome size does not correlate with body size in multicellular organisms that differ largely in cell number. Weak correlations between genome size and body size may occur if body size is related to both cell size and number (a situation intermediate between B and C).

Figure 4

Representative pictures of relatively large multicellular organisms, including decapod crustaceans, bony fishes, ferns and flowering plants [232,233,234,235] that show positive (+) relationships between genome size and reproductive propagule size, but no (0) or weakly negative (−) relationships with adult body size (Table 1 and Table 2), largely following predictions #1, #3 and #4 of the Single-Cell ‘Bottleneck’ Hypothesis (SCBH: Table 6). These relationships occur apparently because genome size is more related to cell size (including the cells of eggs, spores and seeds) than to cell number (which mainly determines the various sizes of relatively large organisms) (following assumptions #2–#5 of the SCBH: Table 6).

Figure 5

Schematic diagrams showing how the size and number of somatic cells (blue circles) in multicellular organisms tend to parallel the size and number of reproductive propagules (here illustrated as eggs: red circles), following prediction #5 of the Single-Cell ‘Bottleneck’ Hypothesis (SCBH: Table 6). (A): An organism with relatively few large somatic cells produces relatively few large eggs. (B): An organism with relatively many small somatic cells produces relatively many small eggs. These differences are similarly produced by changes in genome size (see Table A2) and ambient temperature (see Section 4.6).

Figure 6

Hypothetical scenarios showing possible causal (functional or evolutionary) relationships among the sizes of reproductive propagules, genomes (DNA content per cell), somatic cells and germ cells. These scenarios, each of which may occur at least in some cases, attempt to explain why the sizes of the above entities are often positively correlated with one another (see Figure 1D, Figure 2D and Figure 4; Table 2, Table 3, Table 4 and Table 5, Table A1 and Table A2). The left-hand scenario hypothesizes that natural selection for larger reproductive propagules with relatively large cells favors larger genomes for structural and functional support. These larger genomes are then passed onto somatic cells and next-generation germ cells, which are also larger because of nucleotypic effects. The larger germ cells, in turn, contribute structurally and functionally to larger next-generation propagules, thus reinforcing the adaptive evolutionary effects. The selection for larger propagules may also be associated with changes in other life-history traits. In addition, changes in the sizes of somatic cells may have secondary effects on other phenotypic traits, including rates of growth, development and metabolism. The middle scenario hypothesizes that spontaneous or environmentally induced changes in genome size affect the sizes of somatic and germ cells, and secondarily propagule size and possibly other associated phenotypic traits. The right-hand scenario hypothesizes that natural selection for larger somatic cells favors larger genomes for structural and functional support. These larger genomes, in turn, support larger germ cells and reproductive propagules with possible secondary effects on other life-history traits. The selection for larger somatic cells may be direct or the indirect result of selection on other associated phenotypic traits. All of the hypothetical scenarios include a single-celled developmental stage, and as such are informed by the Single-Cell ‘Bottleneck’ Hypothesis (SCBH) described in Table 6.

Figure 7

Body-mass scaling of egg mass and number per clutch (left-hand graphs) (data from [101]), and body-length scaling of genome size (right-hand graphs) (data from [57]) in copepods and decapods having different ratios of juvenile/adult mortality (M_J/M_A) (data from Table A3). For copepods, the top ratio is based on M_J for nauplii, whereas the bottom ratio is based on M_J for copepodids. The scaling exponent (slope, b) is indicated for each relationship. Hypothetical effects of M_J/M_A on the observed scaling relationships are discussed in Section 4.7.1 (also see [101]).