Somatic polyploidization and cellular proliferation drive body size evolution in nematodes

Abstract

Most of the hypodermis of a rhabditid nematode such as Caenorhabditis elegans is a single syncytium. The size of this syncytium (as measured by body size) has evolved repeatedly in the rhabditid nematodes. Two cellular mechanisms are important in the evolution of body size: changes in the numbers of cells that fuse with the syncytium, and the extent of its acellular growth. Thus nematodes differ from mammals and other invertebrates in which body size evolution is caused by changes in cell number alone. The evolution of acellular syncytial growth in nematodes is also associated with changes in the ploidy of hypodermal nuclei. These nuclei are polyploid as a consequence of iterative rounds of endoreduplication, and this endocycle has evolved repeatedly. The association between acellular growth and endoreduplication is also seen in C. elegans mutations that interrupt transforming growth factor-beta signaling and that result in dwarfism and deficiencies in hypodermal ploidy. The transforming growth factor-beta pathway is a candidate for being involved in nematode body size evolution.

Figure 1

Body size has evolved repeatedly within the Rhabditida. Species: Acrobeloides maximus (A. m.), Acrobeloides nanus (A. n), Panagrellus redivivus (Pu. re.), Panagrolaimus rigidus (Pa. ri.), Rhabditoides regina (Rh. r.), Caenorhabditis elegans (C. e.), Oscheius dolichuroides (O. d.), Oscheius sp. (DF5000) (O. sp.), Oscheius myriophila (O. m.), Rhabditella octopleura (R. o.), Pellioditis sp. (EM434) (Pe. sp.), and Pellioditis typica (Pe. t.). All species are depicted at young adulthood. Numbers correspond to nodes used in comparative contrasts analysis.

Figure 2

Evolution of nuclear DNA content. Oscheius sp. (DF5000) (A and C) and O. myriophila (B and D) differ in adult hypodermal DNA content at late adulthood. (A and B) Reconstructions of nematode nuclei based on confocal images of whole-mounted nematodes; white arrows indicate hypodermal nuclei (surrounded by larger intestinal and smaller neuronal nuclei). (C and D) Distribution of densitometrically estimated DNA contents of hypodermal nuclei; black arrowheads are means.

Figure 3

The relationship between nucleus number and body size. (Left) Comparison of species means (log transformed). Hypodermal nuclear number at adulthood is from Cunha et al. (15); maximum body volume is at adulthood. (Right) Phylogenetic contrasts of the same data. See text for regression statistics. Species and contrasts as in Fig. 1.

Figure 4

The relationship between the product nucleus number × ploidy and body size. (Left) Comparison of species means (log scale). (Right) Phylogenetic contrasts of the same data. See text for regression statistics. Species and contrasts are as in Fig. 1.

Figure 5

Body size mutants in C. elegans, depicted at 96 h after hatching. daf-4 and sma-2 encode components of a transforming growth factor-β (TGF-β) signaling pathway; dpy-2 encodes a cuticle collagen.