Complex sperm evolution.

A world without sexual selection would be a somber place, lacking the rich medley of stimulating sights, sounds, and smells that help individuals win the evolutionary prize of reproductive success. Sexual selection was Darwin’s second great idea (1), and we recognize it as a potent and widespread evolutionary force that probably interacts across the whole genome (2). We also recognize that sexual selection penetrates far beyond mating: females of most species mate with multiple males, generating additional selection from sperm competition (3) and the option for cryptic female influences on fertilization (4). With this greater depth and breadth of importance for sexual selection, modern evolutionary biologists have been facing questions similar to those that confronted Darwin and discovering an exciting diversity in reproductive form and function at the intimate level of the gamete (5). In PNAS (6), a comparative study of closely related water beetles reveals this diversity through a remarkable complexity of adaptations in sperm form and function, and analyzes their coevolution with an equally remarkable elaboration in female reproductive tract architecture. Although the uniform function for a sperm cell is fundamentally to transport the male haplotype to the female pronucleus, the diversity of sperm form and function is far from uniform. The size range alone is huge across the animal kingdom: the porcupine’s 28-μm sperm (7) contrasts dramatically with the current world record holder Drosophila bifurca, whose spermatozoal leviathans stretch to 6 cm (8). Maintaining the species-specific sperm size range seems to be vital: nutritional limitation that halves the resources available for males to invest in gametogenesis leads to a halving in the number of sperm produced but no reduction in the size of the sperm (9). Why this 2,000-fold variation in sperm size across species, when all have the same fundamental task? Comparative analyses across some groups show that variation in relative sperm size is influenced by postcopulatory sexual selection: males in species in which females have mating patterns that generate sperm competition have evolved relatively longer spermatozoa (10). What gives longer sperm a competitive advantage? If longer sperm allow faster swimming velocities, more powerful propulsive forces, or greater resource provision to these behaviors, then postcopulatory sexual selection could favor sperm elongation, but only as long as the female has evolved a competitive arena demanding these functions. In support of a female role here, a number of comparative studies, including across beetles (11), have found associations between sperm size and female reproductive tract morphometry (10). However, why should females diversify fertilization arenas, when, again, the fundamental function of such environments is simply to ensure the presence of fertile sperm at the right time for fertilization? Classic sexual selection theory would argue that females should evolve an arena that provides honest information about the condition or quality of the males struggling to win within it. There is no reason why this should be restricted to the demanding development of stunning plumage or enormous antlers, because honest signaling information could be as easily gleaned by females at the level of the gamete, well after matings. Selection experiments with Drosophila melanogaster provide support for this theory: after divergently selecting replicate populations in both sperm length and female tract length, the advantage to males with longer sperm only existed when the sperm were competing in a reproductive tract that had also been elongated (12). The male sperm trait is therefore only advantageous when its competitive arena is specifically selective. In Drosophila, a natural link between sperm length and male condition exists, because the production of longer sperm is demanding of male resources and maturation time (13). Female fruit flies therefore derive an honest signal of male ability and condition by simply evolving a fertilization arena that gives a fertilization advantage only to those males that can produce long sperm. It was this background that allowed Miller and Pitnick to conclude that “Giant sperm tails are the cellular equivalent of the peacock’s tail” (12). A number of studies have therefore shed light on the evolution of sperm size by sexual selection (10, 12); what about the evolution of sperm architectural complexity? Spermatozoa exhibit the greatest Fig. 1. Sperm conjugates forming the complex rouleaux of the dytiscid water beetle Neoporus undulates. Left: Epiflourescence image of a single conjugate illustrating the stacking of more than 50 fluorescing sperm heads. The concave shape of the sperm heads allows the cells to stack neatly together, as illustrated in a transmission electron microscopy cross-section through the rouleau (Right), where each concentric ring is an individual sperm head. Image courtesy of Dawn Higginson (Syracuse University). Fig. 2. The elaborate female reproductive tract of Ulvarus lacustris, a 2-mm-long dytiscid water beetle, illustrating the brown bulb-shaped spermetheca, where sperm are stored after mating, and the elongate spermathecal duct, down which sperm must pass to fertilize. Image courtesy of Scott Pitnick (Syracuse University).