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Life-History Change in Disease-Ravaged Tasmanian Devil Populations

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Life-History Change in Disease-Ravaged Tasmanian Devil Populations Life-history change in disease-ravaged Tasmanian devil populations Menna E. Jones*†‡§, Andrew Cockburn†, Rodrigo Hamede*, Clare Hawkins*¶, Heather Hesterman*, Shelly Lachishʈ, Diana Mann‡, Hamish McCallum*, and David Pemberton¶ *School of Zoology, University of Tasmania, Hobart TAS 7001, Australia; †School of Botany and Zoology, Australian National University, Canberra ACT 0200, Australia; ‡Wildlife Management Branch and ¶Biodiversity Conservation Branch, Department of Primary Industry and Water, Hobart TAS 7001, Australia; and ʈSchool of Integrative Biology, University of Queensland, St. Lucia QLD 4072, Australia Edited by James H. Brown, University of New Mexico, Albuquerque, NM, and approved April 17, 2008 (received for review November 28, 2007) Changes in life history are expected when new sources of extrinsic mortality impact on natural populations. We report a new disease, devil facial tumor disease, causing an abrupt transition from iteroparity toward single breeding in the largest extant carnivo- rous marsupial, the Tasmanian devil (Sarcophilus harrisii), in which males can weigh as much as 14 kg and females 9 kg. This change in life history is associated with almost complete mortality of individuals from this infectious cancer past their first year of adult life. Devils have shown their capacity to respond to this disease- induced increased adult mortality with a 16-fold increase in the proportion of individuals exhibiting precocious sexual maturity. These patterns are documented in five populations where there are data from before and after disease arrival and subsequent population impacts. To our knowledge, this is the first known case of infectious disease leading to increased early reproduction in a mammal. The persistence of both this disease and the associated life-history changes pose questions about longer-term evolution- ary responses and conservation prospects for this iconic species. Fig. 1. Tasmanian devil facial tumor disease, a recently emerged infectious cancer, has caused virtual semelparity and a dramatic increase in the propor- tion of juvenile females breeding. carnivorous marsupial ͉ infectious cancer ͉ wildlife disease ͉ precocious breeding ͉ semelparity persists at very low population densities suggests that the disease ECOLOGY hanges in life history are expected when new sources of may be strongly frequency-dependent (10). Frequency- Cextrinsic mortality impact on natural populations (1, 2). In dependent diseases do not burn out at low host density and can age-structured populations, juvenile survival and age at first cause extinction (15). Indications of frequency dependence and reproduction respond rapidly to changes in density, followed by predictions from two different types of population modeling, changes in fecundity (3, 4). Adult survival is influenced by combined with estimated rates of ongoing spread, have led to phenotypic effects on juveniles and is the last vital rate to be concerns that extinction in the wild is a possibility in 20–25 years’ affected (3, 4). Life-history change has been documented in time (10). That this novel disease could have catastrophic response to release from culling pressure (4), an increase in consequences for the Tasmanian devil is an unfortunate coin- fishing pressure (2), and changes in predator assemblage and cidence of loss of genetic diversity at a functional gene region and level of predation (1, 5). Early reproduction as a consequence of aggressive mating-season behavior in a carnivore that frequently parasitism has been predicted theoretically (6), with limited inflicts penetrating wounds with its canine teeth. supporting empirical evidence (7, 8). Here, we report a new In this article, we investigate changes in life history in Tas- disease, devil facial tumor disease (DFTD) (Fig. 1), causing an manian devil populations affected by the facial tumor disease. abrupt transition from iteroparity toward single breeding in the We analyzed data from five study sites where individually largest extant carnivorous marsupial, the Tasmanian devil (Sar- marked devil populations have been studied both before and cophilus harrisii). Endemic to the Australian island of Tasmania, after the arrival of the disease. Changes in precocial sexual male Tasmanian devils can weigh as much as 14 kg and females maturity are documented in relation to changes in population 9 kg. To our knowledge, this is the first known case of infectious age structure and consequent lifetime number of breeding events disease leading to increased early reproduction in a mammal. that result from the disease-induced increase in adult mortality. Symptoms resembling DFTD were first reported in 1996 and by 2007 had spread over more than half of the species’ range on Results the island of Tasmania (Fig. 2), including the majority of Disease has had a highly significant effect on the age structure higher-density populations (9, 10). Populations affected by of the devil populations at all five sites (␹2 ϭϪ5.52, df ϭ 1, P Ͻ DFTD have suffered declines as great as 89% (9, 10). This consistently fatal disease is an infectious cancer, thought to be transmitted by allograft, with tumor cells spread directly between Author contributions: M.E.J. designed research; M.E.J., R.H., C.H., H.H., S.L., D.M., and D.P. devils through biting (11, 12). Very low diversity in MHC genes, performed research; M.E.J. and H.M. analyzed data; and M.E.J. and A.C. wrote the paper. which play a key role in immune response to tumors and grafts, The authors declare no conflict of interest. enables transmission (13). The tumors primarily affect adults This article is a PNAS Direct Submission. (animals Ն2 years old) and cause death within months. Evidence §To whom correspondence should be addressed at: School of Zoology, University of that most penetrating biting injuries occur among adult males Tasmania, Private Bag 5, Hobart TAS 7001, Australia. E-mail: [email protected]. and females in the mating season (14) and that the disease © 2008 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0711236105 PNAS ͉ July 22, 2008 ͉ vol. 105 ͉ no. 29 ͉ 10023–10027 Downloaded by guest on September 25, 2021 Mt. William (1996) Wisedale (2006) Freycinet peninsula (2001) Little Swanport (1999) Pawleena (2002) 0150 00200 Kilometres Fig. 2. Study sites in relation to current distribution of DFTD. A year in brackets is the year in which the disease was first detected at each site. Stars represent the known westernmost distribution of the disease in 2007. 0.001), with a much higher proportion of older (3ϩ years) 2000 at Freycinet) of 1-year-old females bred. After the disease animals present in the population before the disease (log odds spread, precocial breeding increased on average 16-fold to ratio of being old vs. young before and after disease ϭϪ1.774, between 13.3% (Mt. William, 2004) and 83.3% (also Mt. Wil- 95% C.I. Ϫ2.428 to Ϫ1.257; Fig. 3a). The final model included liam, 2006), except at Little Swanport, where it remained at zero. only disease (fixed effect) and between-year variation within site The final model included only disease (fixed effect) and be- (random effect). There were no consistent differences between tween-year variation within site (random effect). There were no sexes (removal of sex term from model: ␹2 ϭ 2.728, df ϭ 1, P ϭ statistically significant differences attributable to site (removal 0.099) or among sites (removal of site term from model: ␹2 ϭ of site term from model: ␹2 ϭ 7.437, df ϭ 4, P ϭ 0.115). 7.663, df ϭ 4, P ϭ 0.105). Before the disease emergence at Freycinet, a significantly Discussion greater proportion of females (21 of a total of 29) produced more The arrival of DFTD on the Freycinet Peninsula in 2001 than one litter in their lifetime than after the disease spread triggered an immediate and steady decline in survival rates (16) across the site (6 of 17; Fisher’s exact test, P ϭ 0.028; Fig. 4). of at least 60% compared with former levels (10), resulting in a Precocial breeding by 1-year-old females increased substantially population comprised almost entirely of animals Ͻ3 years of age. after disease emergence (log odds ratio of 1-year-old breeding vs. Before the disease, the modal female began seasonal breeding at not breeding before and after disease ϭϪ3.2797, 95% C.I. age 2 and produced a litter annually for 3 years, with senescence Ϫ5.147 to Ϫ1.728; ␹2 ϭϪ4.057, df ϭ 1, P Ͻ 0.001; Fig. 3b). and death occurring in her fifth or sixth year (M.E.J., unpub- Before the disease, between zero (at three sites) and 12.5% (year lished work) (17, 18). Females now generally have one breeding 10024 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0711236105 Jones et al. Downloaded by guest on September 25, 2021 a 60 40 20 % 3+ year old devils in population 0 male male male male male female female female female female b 100 80 60 40 20 % one year old females breeding 0 female female female female female Freycinet Mt William Little Swanport Pawleena Wisedale Site Fig. 3. Changes in life-history traits of Tasmanian devils (Sarcophilus harrisii) in response to invasion by DFTD at five sites across eastern Tasmania. Filled bars, before disease; open bars, after disease emergence. Sample sizes are provided in Methods.(a) Proportions of all males and all females 3 years or older before and after the appearance of the disease. (b) Proportion of 1-year-old females breeding in populations before and after arrival of the disease. ECOLOGY opportunity and may not survive long enough to rear that litter. with age, selection for early reproduction will occur (6). Demo- Hence, they are now largely semelparous. graphic responses can, over time, evolve into new, genetically Comparable changes in age structure have occurred at four mediated life-history parameters (1).
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