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Understanding the relationship between life-history patterns, population dynamics and population regulation has been a central issue of population ecology for the better half of a century (Cole 1954; Sinclair 1989). Despite this, the consequences of infectious diseases and disease-induced changes to host life histories for population dynamics have only recently begun to receive attention (Choisy & Rohani 2006; Woodroffe et al. 2008).
Infectious diseases that reduce population numbers or densities can cause density-dependent changes in host population dynamics as a result of changes to the life-history traits of individuals in the population (Fowler 1981). Demographic responses to perturbations that cause a reduction in population size include increased reproductive rates, earlier onset of sexual maturity, increased survival of some population classes, or increased recruitment rates (Coulson et al. 2004). These compensatory changes in life-history traits can confer animal populations with a remarkable capacity to recover from perturbation and have rescued populations from the brink of extinction (for example, black-footed ferrets Grenier, McDonald & Buskirk 2007). However, while compensatory responses to changes in population abundance and density are known for long-lived species (Pistorius et al. 2001; Hadley et al. 2006) and have been extensively studied in species subject to harvesting (Coulson et al. 2004; Choisy & Rohani 2006, Milner, Nilsen & Andreassen 2007), such responses to disease epidemics remain largely unexplored (Loison, Gaillard & Jullien 1996; Mutze et al. 2002).
Moreover, knowledge of the demographic changes that stem from disease epidemics is essential not only for understanding the processes that affect population dynamics but also for effectively managing diseased populations. Since infectious diseases are potentially important drivers of local population extinctions (Haydon, Laurenson & Sillero-Zubiri 2002; Gerber et al. 2005), management actions are often needed to mitigate the detrimental impacts of disease, particularly for species of conservation concern. Understanding the impact of a pathogen on host population dynamics and host life histories is necessary to predict population responses to disease control measures (McCallum, Barlow & Hone 2002).
Devil facial tumour disease (DFTD) is a recently emerged infectious cancer that is now widespread and represents a serious threat to the Tasmanian devil Sarcophilus harrisii, (Hawkins et al. 2006). This fatal cancer is transmitted from animal to animal as an allograft (a tissue graft of the actual tumour cells) during social interactions (Siddle et al. 2007). Estimates of disease spread, indicating that DFTD will cover the entirety of the devils’ range in as little as 5 years time, in combination with models predicting population declines to extinction within 15 years of disease arrival, equate to an unacceptable risk of extinction for the wild devil population (McCallum et al. 2007).
Recently, Jones et al. (2008) examined changes in life history in five Tasmanian devil populations affected by the facial tumour disease, reporting consistent changes to population age structure and a decline in the age of sexual maturity of females across all five populations. Their study was based on snapshots of 1 or 2 years data ‘before’ and ‘after’ an unknown disease arrival time at each site, as this is the only information available at multiple sites. Here we report the results of a demographic study conducted at one of the five sites, the Freycinet Peninsula on the east coast of Tasmania. This site has been intensively trapped since 1999 with disease first appearing in 2001. The arrival of DFTD in the Freycinet Peninsula population triggered an immediate and steady decline in the survival rates of adults and sub-adults, and resulted in a substantial reduction to population growth rate and an ongoing decline in population abundance (Lachish, Jones & McCallum 2007). This unique data set allows us to investigate thoroughly the demographic and life-history changes following disease arrival, accounting for initial demographic variability within a population before disease arrival and subsequently monitoring changes in life-history parameters with disease progression.
In this study, our objectives were (i) to determine the nature of disease impacts on population demographic parameters and life-history traits, (ii) to obtain robust estimates of the vital rates of diseased and nondiseased individuals for use in models to aid management actions, and (iii) to determine the population's ability to respond to low population densities and to compensate for the detrimental impacts of DFTD.
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The arrival of DFTD to the Freycinet Peninsula resulted in a substantial change to the age structure of the population, caused by the loss of older individuals. This shift to a younger population age structure is a result of disease-driven declines in adult survival rates of Tasmanian devils (Lachish et al. 2007) and represents a direct population level consequence of disease impacts on individuals. That the decline in mean age class was not wholly explained by disease prevalence and did not begin immediately upon disease arrival (despite adult survival rate declining at this time, Lachish et al. 2007), is likely to be a consequence of spatial variation in disease impacts associated with disease spread. Since DFTD reached the southernmost tip of the 30-km long Freycinet Peninsula approximately 5 years after its initial detection (Hawkins et al. 2006; McCallum et al. 2007), older individuals would have been able to survive and persist in unaffected areas for several years before disease spread to those areas. The initial increase in the mean age of the population may be a result of a high recruitment or immigration pulse before the commencement of the study.
The loss of adults from a population can pose serious threats to its persistence by reducing the breeding potential of the population either as a consequence of lowered reproductive success or recruitment rates (Coltman et al. 2003) or as a result of breakdowns to social or dominance hierarchies and networks (Rogers et al. 1998). If, however, there is a concurrent reduction in population abundance, which reduces competition for normally limited resources, then these potential impacts may be mitigated by compensatory changes in demographic parameters, such as an earlier onset of maturity or increased fecundity (Coulson et al. 2004).
We observed an increase in the proportion of 1-year-old females breeding as disease progressed through the population, providing evidence of reproductive compensation in Tasmanian devil populations in response to disease-driven declines in adult survival rates and population abundance. In contrast, neither litter size nor reproduction by adult females showed evidence of compensatory responses to population decline following disease arrival. Since a very high proportion of adult females bred each year (often only the old, senescent, females did not breed), and since Tasmanian devils produce super-numerary young (females give birth to more than 20 neonates, Hughes 1982), it seems there is limited scope for compensatory increases in these reproductive traits, as selection has already maximized females’ investment in these life-history parameters. For ‘fast-living’ species, such as the Tasmanian devil, that mature early and have high fecundity rates, the decrease in generation time resulting from the earlier onset of sexual maturity, will be key to maximizing the reproductive output of the population and its population growth rate (Oli & Dobson 2003). The plasticity observed in the age of first reproduction in Tasmanian devils and the capacity for this life-history trait to respond to changes in population density potentially represent an important mechanism for mitigating population perturbations.
The earlier onset of maturity in Tasmanian devils breeding in the diseased population appeared to be facilitated by more rapid growth in response to reduced population density, via reduced food competition. It is widely recognized that increases in food availability and consequent nutritional status of individuals’ result in increased growth rates of individuals (see Altmann & Alberts 2005 and references therein) which can also accelerate sexual maturity (Bercovitch & Strum 1993). In this study, we detected a significant increase in the growth rates of 1-year-old males over time (with suggestion of a similar trend in females), thus demonstrating that growth rates did increase as the population declined, most likely in response to increased food availability. Although, it is difficult to ascertain the extent of density-dependent effects on vital rates before disease arrival, models showing that the population growth rate of the Freycinet population was stable pre-disease suggest that the population was initially close to carrying capacity (Lachish et al. 2007). Life-history theory predicts that resource limitation at higher population densities will more adversely affect body growth in the larger sex (Hedrick & Temeles 1989).
The finding that female growth rates were not as strongly influenced by changes in population abundance indicates that the ability to breed as a 1-year-old (precocial breeding) is influenced by more than just population density. In fact, our data suggest that, in addition to density-dependence, the age of first reproduction in Tasmanian devils is determined by the ability of individuals to attain a critical size for sexual maturity in their first year. This is indicated by the extremely strong relationship between body size and the probability of 1-year-olds breeding, the absence of precocial breeders in 2007 when, although population density was at its lowest, 1-year-olds were significantly smaller than average, together with the lack of strong support for models relating precocial breeding to either trend or disease prevalence (as indicators of changing population density).
Since Tasmanian devils are seasonal breeders (Pemberton 1990), there will likely be a time limit by which a critical size for maturity must be reached for breeding to occur in a given season. Consequently, the timing of reproduction will have a great effect on the likelihood that an individual will be large enough to breed in its first year. Devils exhibit a seasonal synchronous peak in reproduction but the breeding season is actually quite broad (births occur from February through June, Pemberton 1990), resulting in a potential disparity in offspring size of up to 20 weeks growth. In addition, 1-year-old breeders do not come into oestrus until late April/May (H. Hesterman, S. Jones & M. Jones, unpublished), presumably the earliest time since weaning in January at which they are able to attain a critical size and sexual maturity. Thus, it seems that some individuals, the offspring of late breeders and particularly 1-year-old breeders, will be less likely to attain the critical size necessary to breed in their first year. Although this conclusion remains to be tested, it may partly explain why we did not record precocial breeding in 2007: most of these individuals would have been the offspring of precocial breeders [more than 50% (12/23) of breeders captured in 2006 were 1 year old] and thus born relatively late in the season. This constraint on the probability that individuals will be large enough to breed in their first year will severely limit the strength of this reproductive compensatory response to declines in population abundance.
In addition to the timing of reproduction, maternal effects, in which the mother's phenotype shapes her offspring's phenotype independent of any genetic effects (Bernardo 1996), may also influence the capacity of females to reach a critical body size and thus, their ability to breed in their first year. Of particular interest is the effect a female's disease status might have on the condition (phenotype) of her offspring. If, as seems likely, the offspring of diseased mothers are adversely affected by her condition (assuming she survives long enough to raise them), then this might also explain the absence of precocial breeding in 2007; since almost half (11/23) the females breeding in 2006 [and 82% (9/11) of adult females breeding in this year] were diseased. We currently lack the necessary data to examine the consequence of maternal disease status for offspring condition and this effect remains to be investigated. Nonetheless, this would appear to further constrain the likelihood that individuals breed as 1-year-olds.
A key result of this study was that diseased females had significantly more female-biased litters than did healthy females, suggesting that DFTD infection leads to sex allocation biases in Tasmanian devils. The theory of adaptive sex allocation states that in polygynous mammals that exhibit reproductive skew, mothers in poor physical condition, or breeding in poor environmental conditions, are expected to invest more in daughters than in sons, since the costs of producing and rearing quality sons are much greater than for producing quality daughters (Trivers & Willard 1973). In humans, studies have shown that diseases (including cancer) can lead to female-biased offspring sex ratios (James 2002). We are not aware, however, of any other study in a nonhuman system that shows that an infectious disease can alter maternal sex allocation or investment in offspring. If the change in offspring sex ratio that accompanied disease infection in this study occurs throughout all disease-affected devil populations, it would provide novel evidence that adaptive, facultative adjustment of offspring sex ratio occurs in response to disease-induced changes in maternal condition in a polygynous mammal. Mechanisms facilitating offspring sex ratio manipulation are still the source of speculation and largely unknown (Johnson & Ritchie 2002; Pike 2005), although studies highlight the role of stress-related disruptions to endocrine function due to environmental perturbation (Pike & Petrie 2006) or the physiological challenge of a disease (James 2001). The possibility that DFTD infection alters hormone levels in devils subsequently affecting pouch young sex ratios clearly warrants further investigation.
A facultative adjustment to female-biased pouch young sex ratios, if propagated through the population, could potentially enhance population growth and assist population recovery because theoretically, the most productive populations are those with a female-biased sex ratio (Caughley 1977). Diseased females, however, may not survive to rear their offspring successfully. It therefore seems doubtful that there will be long-term consequences for the population dynamics or persistence of this population as a result of the change in this life-history parameter.
This study found that an epidemic of an infectious disease resulted in major changes to both population age structure and life-history parameters of Tasmanian devils. Reproductive compensation occurred in response to disease impacts via an increase in precocial breeding. The strength of this compensatory response, however, was shown to be limited by factors such as the timing of reproduction and maternal effects, which constrain the ability of offspring to reach a critical size for maturity within the time frame dictated by the annual breeding season. Constraints on the ability of individuals to breed as 1-year-olds mean that most individuals in this population will have only one opportunity to breed in their lifetime, at 2 years of age. The average age of diseased individuals in this population is 2·27 (95% CI 1·99–2·56) years. Since individuals rarely survive for more than 6 months with disease (Lachish et al. 2007) and juveniles only gain independence at 9 months of age, these adults will be unlikely to rear that one litter successfully and thus reproductive success and recruitment will be low.
With precocial breeding reliant on rapid growth in the first year, the opportunity for selection to favour fast-growing individuals that are able to breed earlier is evident, provided there is a heritable basis for rapid early growth in devils. The Freycinet population of devils now exhibits many of the conditions necessary for selection to favour early reproduction (Charnov & Schaffer 1973; Jones et al. 2008), with substantial reductions in adult survival rates (Lachish et al. 2007) and higher disease prevalence among adults than young individuals (H. McCallum, M. Jones, C. Hawkins, R. Hamede, S. Lachish, D. Sinn, N. Beeton & B. Lazenby, unpublished). The possibility that evolution will drive a shift towards this new life-history pattern in Tasmanian devils potentially increases the likelihood of future population persistence and supports a growing body of evidence indicating that infectious diseases may be strong selective forces for life-history variation and evolution in a range of taxa (Altizer, Harvell & Friedle 2003; Todd 2007; Bolker et al. 2008).