Worm Breeder's Gazette 17(3): 36 (November 1, 2003)

These abstracts should not be cited in bibliographies. Material contained herein should be treated as personal communication and should be cited as such only with the consent of the author.

Evolution of sex differences in lifespan in nematodes

Diana McCulloch, David Gems

Department of Biology, University College London, Gower Street, London WC1E 6BT

N2 males live ~20% longer than hermaphrodites when maintained in isolation to prevent deleterious interactions with other worms (1). We have found that this is also true of 9/12 other C. elegans wild isolates tested. Increased male lifespan is therefore typical of C. elegans as a species, and not unique to N2. Why might this male longevity bias have evolved? One possibility is that it is a consequence of protandrous hermaphroditism, which is likely to lead to a skew in the male reproductive probability distribution to later ages. The evolutionary theory of aging suggests that this would result in the evolution of greater longevity in males. To test this idea, we measured the lifespans of both sexes of four dioecious and three more hermaphroditic terrestrial nematode species. However, males proved to be significantly longer-lived than hermaphrodites/females in all other nematode species tested, bar one. This disproved our hypothesis, and suggested that a male longevity bias is typical of free-living nematodes. The exception was C. briggsae, since hermaphrodites were significantly longer-lived than males in the three isolates tested, G16, HK104 and VT847. This could be an evolutionary consequence of the fact that following mating in this species, oocytes are preferentially fertilised by X-bearing sperm, so that outcross progeny are initially mainly hermaphrodites (2). Given that the frequency of males among progeny of selfing hermaphrodites is comparable to that in C. elegans (3), it seems likely that C. briggsae males are exceptionally rare in the wild. Potentially, this rarity results in reduced selection against deleterious mutations with male-specific effects, and the evolution of reduced male longevity. Interestingly, lifespans of males of dioecious species as a whole were greater than those of males of hermaphroditic species (p < 0.001); females were not longer-lived overall than hermaphrodites. Thus, the rarity of males in hermaphroditic species may lead to the evolution of reduced male lifespan.

Male C. elegans are also more likely to form dauer larvae than hermaphrodites (4). We have found that insulin/IGF-like signalling plays a role in both increased male dauer formation and lifespan in this species. Possibly increased male lifespan evolved due to selection for increased dauer formation. Yet in other species tested we saw increased dauer formation in hermaphrodites/females, arguing against this idea. However, since this included C. briggsae, where hermaphrodites are the longer-lived sex, it is possible that common mechanisms underlie the evolution of sex differences in dauer formation and lifespan in the genus Caenorhabditis.

Why might male free-living nematodes of both hermaphroditic and dioecious species be longer-lived than the feminine sex? Within a species, the sex experiencing greater extrinsic mortality is expected to become the one with more rapid aging (5). One cause of early mortality in C. elegans hermaphrodites is internal hatching of eggs (bagging). If bagging occurs at significant rates in terrestrial nematodes, the resulting bias in sex-specific survival could account for the evolution of the male longevity bias. Using a simple starvation test, we observed varying levels of bagging in six other terrestrial nematodes tested. In conclusion, a male longevity bias is common among dioecious and hermaphroditic terrestrial nematode species, and may have evolved as a consequence of bagging, while reduced male longevity in hermaphroditic relative to dioecious species may have evolved as a consequence of male rarity.

(1) Gems & Riddle (2000) Genetics 154: 1597; (2) LaMunyon & Ward (1997) PNAS 94: 185; (3) Nigon & Dougherty (1949) J. Exp. Zool. 112: 485; (4) Ailion & Thomas (2000) Genetics 156: 1047; (5) Williams (1957) Evolution 11: 398