Andrew Cockburn,* Ian M. Mansergh,? ... Address for correspondence and reprints: Andrew Cockbum, Department of Zoology, Australian .... M. S. BOYCE, ed.
Letter to the Editor Molecular Clocks and Generation Time in Burramyid Marsupials’ Andrew Cockburn,* Ian M. Mansergh,? Linda S. Broome,$ and Simon Ward4 *Department of Zoology, Australian National University; tDepartment of Conservation, Forests and Lands, Victoria, Northern Territory; $Kosciusko National Park, New South Wales; $Department of Zoology, Monash University, Australia
Controversy surrounds the extent to which the clocklike rate of base changes in DNA is influenced by the generation time of the organisms involved. For example, a comparatively high rate of nucleotide substitution in rodents has been attributed to their short generation time compared with that of primates (Wu and Li 1985). Springer and Kirsch (1989) have recently documented a rate slowdown among marsupials in the family Burramyidae. They argue that burramyids have a short generation time relative to other phalangeriforms and that they hence represent “a striking counterexample to the common view that rates of change in DNA sequences are inversely correlated with generation time” (Springer and Kirsch 1989, p. 331). Springer and Kirsch (1989) concede that demographic data are sketchy, at best, for most phalangeriform marsupials. In this note we comment on the demographic and reproductive data necessary for assessment of generation time, and we present evidence of extraordinary longevity in free-living populations of both genera (Burramys and Cercartetus) which can be unequivocally assigned to the burramyids. We would urge caution in use of this group as falsification of a relation between generation time and the rate of DNA evolution. Accurate measurement of generation time is confounded by many difficulties. At least four types of data would be desirable: age at first reproduction, age-specific distribution of births, age-specific survival, and age-specific changes in parental ability. For example, increased lifetime reproductive success of many birds and mammals is highly correlated with life span (Clutton-Brock 1988; Newton 1989). However, in at least some studies, the successful long-lived animals gain an additional advantage not predicted by their life span alone, perhaps because their ability as parents increases with age (e.g., see Coulson and Thomas 1985). Only two types of summary data-age at first reproduction and maximum life span-are available for sufficiently many species of marsupials to permit comparison between the clades studied by Springer and Kirsch. Even then, the laboratory data used by Springer and Kirsch to compare generation times are likely to be very misleading. Few animals live as long in natural circumstances as they do in captivity, and in many cases the seasonal cues that delay the onset of reproduction in the wild are absent in the laboratory. In an extreme example, male marsupials from the genus Antechinus will live for several years in the laboratory, yet in the wild they never live longer than 12 mo, as all males die after a short rut toward the end of their first year of life (Lee and Cockbum 1985). Unfortunately, very few field studies of marsupials have lasted sufficiently long to incorporate the life span of entire cohorts, and this is particularly true of the tropical species that dominate the sample used by Springer and Kirsch. However, old, heavy Pseudocheirus peregrinus are much more successful than younger animals (Pahl 1987), so age at first reproduction is likely to underestimate rates of population turnover. In 1. Key words: molecular clock, marsupial evolution, generation time. Address for correspondence and reprints: Andrew Cockbum, Department of Zoology, Australian National University, GPO Box 4, Canberra City, Australian Capital Territory 2601 Australia. Mol. Biol. Evol. 7(3):283-285. 1990. 0 1990 by The University of Chicago. All rights reserved.
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addition, age at first reproduction does not vary greatly among most phalangeriforms, with onset dominated by seasonality, and occurring at 1 year or 2 years of age, as observed by Springer and Kirsch. The maximum life span of most very large species remains unknown, particularly where there are no obvious criteria by which the age of old animals can be determined. It is more surprising that, although burramyids attain reproductive maturity quickly and are small, so that allometric considerations predict a short life span, no study has successfully set a limit on maximum longevity in this group. Indeed, at least one female tagged as an adult lived the full duration of a lo-year study of B. parvus at Mount Hotham, Victoria, without any sign of a senescent decrease in reproductive output (Mansergh 1989). The population studied occupies prime habitat for this species. Males do have shorter life spans (-4 years), probably as a result of a costly seasonal migration enforced by dominant females (I. M. Mansergh and L. S. Broome, unpublished data). A 4-year study of a low-density population at Kosciusko National Park, New South Wales, has also failed to encompass the life span of females (L. S. Broome, unpublished data). We know of no other same-sized eutherian or marsupial insectivore or granivore (except for the Chiroptera) with a comparable free-living life span. Demographic data for Cercartetus are less satisfactory. Consecutive studies of a high-density population of C. nanus at Wilson’s Promontory National Park in Victoria include females that lived for at least 3 years and males that lived for at least 4 years (S. Ward, unpublished data). During a 7-year study of other small mammal species at the Monga State Forest in New South Wales, a male C. nanus lived for at least 5 years in marginal habitat for this species (A. Cockburn, unpublished data). Its ultimate disappearance coincided with a population decline, and there was no evidence of replacement by younger animals. In almost all marsupials, females survive better than males (Cockburn, accepted), suggesting that maximum female life span may be much greater than 5 years. Because the studies we have briefly reviewed include a range of densities and ecological conditions, from cool temperate rainforest (C. nanus) and coastal shrubland (C. nanus) to alpine boulder fields (B. parvus), taxonomic affinity appears to be more influential than either habitat or density, and we conclude that long life span is likely to be a general characteristic of burramyids. The same long life is not evident in the best available demographic data for free-living dasyurids (Lee and Cockburn 1985), didelphids (Eisenberg 1988), peramelids (Stoddart and Braithwaite 1979), petaurids (Smith 1984; Suckling 1984), pseudocheirids (Pahl 1987), Tarsipes (Wooller et al. 198 l), and at least some small macropods (Christensen 1980). Life spans similar to those of female Burramys occur in Phascolarctos (Lee and Martin 1988) and in phalangerids, which &an live as long as 12 years in the wild (Bell 198 1; Clout and Efford 1984). Only large macropods are definitely known to live for longer periods (e.g., see Norbury et al. 1988), though the same is probably true of vombatids. These data suggest that the generation time of burramyids may be rather long compared with that of many other marsupials, including several families of phalangeriforms. The slowdown of the rate of nucleotide replacement in the burramyids reported by Springer and Kirsch is certainly of interest, and we concur that the study of variation in the rates of DNA evolution requires a pluralistic approach. However, such a pluralistic analysis will require better-quality fundamental biological data than are currently available if we are to distinguish alternative hypotheses. For example, Springer and Kirsch speculate that the extensive torpidation exhibited by all burramyids may retard single-copy DNA evolution by affecting cell turnover in the gametic cell line. Alternatively, slow cell turnover in the soma may facilitate increased life span and therefore may increase generation time. Until better demographic data are available, we would caution against using the burramyids as a strong counterexample to an effect of generation time on DNA evolution.
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LITERATURE CITED BELL,B. D. 198 1. Breeding and condition of possums Trichosurus vulpecula in the Orongorongo Valley, near Wellington, New Zealand, 1966- 1975. Pp. 85- 139 in B. D. BELL,ed. Proceedings of the 1st symposium on marsupials in New Zealand. Zoology Publications from the University of Wellington, no. 74. University of Wellington Press, Wellington, New Zealand. CHRISTENSEN,P. 1980. The biology of Bettongia penicillata Gray, 1837, and Macropus eugenii (Desmarest 18 17) in relation to fire. Forestry Dept. of WA, Bull 9 1. CLOUT, M. N., and M. G. EFFORD. 1984. Sex differences in the dispersal and settlement of brushtail possums (Trichosurus vulpecula). J. Anim. Ecol. 53:737-749. CLUTTON-BROCK,T. H. 1988. Lifetime reproductive success. University of Chicago Press, Chicago. COCKBURN,A. Sex ratio variation in marsupials. Aust. J. 2001. (accepted). COULSON,J. C., and C. THOMAS. 1985. Differences in the breeding performance of individual kittiwake gulls, Rissa tridactyla. (L.). Pp. 489-503 in R. M. SIBLY and R. H. SMITH, eds. Behavioural ecology: ecological consequences of adaptive behaviour. Blackwell Scientific Publications, Oxford. EISENBERG,J. F. 1988. Reproduction in polyprotodont marsupials and similar-sized eutherians with a speculation concerning the evolution of litter size in mammals. Pp. 29 l-3 10 in M. S. BOYCE,ed. Evolution of life histories of mammals: theory and pattern. Yale University Press, New Haven and London. LEE, A. K., and A. COCKBURN.1985. Evolutionary ecology of marsupials. Cambridge University Press, Cambridge. LEE, A. K., and R. W. MARTIN. 1988. The koala: a natural history. New South Wales University Press, Sydney. MANSERGH,I. M. 1989. The ecology and conservation of the marsupial pygmy possum Burramys parvus (Burramyidae, Marsupialia) in Victoria with comparisons to populations in New South Wales. Unpublished Ph.D. thesis, Latrobe University. NEWTON, I. 1989, Lifetime reproductive success in birds. Academic Press, New York. NORBURY, G. L., G. M. COULSON,and B. L. WALTERS. 1988. Aspects of the demography of the western grey kangaroo, Macropus fuliginosus melanops, in semiarid north-west Victoria. Aust. Wildl. Res. 15:257-266. PAHL, L. I. 1987. Survival, age determination and population age structure of the common ringtail possum, Pseudocheirus peregrinus, in a Eucalyptus woodland and a Leptospermum thicket in southern Victoria. Aust. J. Zool. 35:625-639. SMITH, A. P. 1984. Demographic consequences of reproduction, dispersal and social interaction in a population of Leadbeaters possum (Gymnobelideus leadbeateri). Pp. 359-373 in A. P. SMITH and I. D. HUME, eds. Possums and gliders. Australian Mammal Society, Sydney. SPRINGER,M. S., and J. A. W. KIRSCH. 1989. Rates of single-copy DNA evolution in phalangeriform marsupials. Mol. Biol. Evol. 6:33 l-34 1. STODDART,D. M., and R. W. BRAITHWAITE.1979. A strategy for utilization of regenerating heathland habitat by the brown bandicoot (Isoodon obesulus; Marsupialia, Peramelidae). J. Anim. Ecol. 48: 165- 179. SUCKLING,G. C. 1984. Population ecology of the sugar glider, Petaurus breviceps, in a system of fragmented habitats. Aust. Wildl. Res. 11:49-75. WOOLLER,R. D., M. B. RENFREE,E. M. RUSSELL,A. DUNNING, S. W. GREEN, and P. DUNCAN. 198 1. Seasonal changes in a population of the nectar-feeding marsupial Tarsipes spencerae (Marsupialia: Tarsipedidae). J. Zool. Lond. 195:267-279. WV, C.-I., and S.-H. LI. 1985. Evidence for higher rates of nucleotide substitution in rodents than in man. Proc. Natl. Acad. Sci. USA 82: 174 1- 1745. WALTER M. FITCH, reviewing editor
Received October 11, 1989; revision received December 13, 1989 Accepted December 15, 1989
