A network of 14 meteorological stations was installed across the Annapurna range before
the 1999 monsoon season, and expanded to 19 stations encompassing 28 rain gauges in
2000. Rainfall is totalled every 30 min. ‘Look-down’ distance rangers and
measure snow depth and total water content, respectively, once a day at high elevations
(.2,500 m in the Greater Himalaya). Only liquid precipitation is measured in the Tibetan
zone, such that the annual (but not the monsoon) total is underestimated here. The data
presented here (Fig. 2b) represent monsoon averages based on the longest record available
from each station.
Apatite ﬁssion-track dating
Following mineral separation, apatites were polished, etched and irradiated. Standard and
induced track densities were determined on Brazil ruby muscovite external detectors
(geometry factor 0.5), and fossil track densities were determined on internal mineral
surfaces. Ages were calculated using z ¼ 359 ^ 20 for dosimeter glass CN-5. All ages are
central ages and are reported with 1
errors. Long-term erosion rates are conservatively
estimated on the basis of the ﬁssion-track age, and assuming a geothermal gradient of
and an annealing temperature of 140 8C.
A 3-arcsec (,90 m) digital elevation model (DEM) is the basis of all topographic analyses.
Hillslope angles are calculated at every pixel in the DEM based on a 3 £ 3 pixel
(,180 £ 180 m) grid. Mean hillslope angles were extracted from a moving, 5-km-radius
window centred on the Marsyandi River. Maximum, minimum and mean elevation (Fig.
2) were calculated along a 50-km-wide swath oriented perpendicular to the strike of the
range and centred on the Marsyandi River (or the Nar-Phu River above its conﬂuence with
Glacial areas were calculated from present and reconstructed ice margins mapped on aerial
photographs, and transferred ﬁrst to 1:50,000 scale topographic maps and then to the
digital topography. Based on glacial hypsometry, equilibrium-line altitudes were
estimated with an assumed accumulation-area ratio of 0.65. To avoid uncertainty
introduced by avalanches on to glaciers from adjacent high peaks, 29 small glaciers (95%
are ,2.5 km
), lacking high headwalls, were analysed. The regional equilibrium-line
altitude gradient shows little sensitivity to accumulation-area ratios ranging from 0.4 to
Speciﬁc stream power
Analysis was focused on catchments ranging from 3 to 7 km
within the non-glaciated part
(,4,200 m elevation) of the study area. These basins drain approximately half of the
landscape and are sufﬁciently large to be ﬂuvial, as opposed to colluvial/debris ﬂow,
channels. Monsoon rainfall was smoothed across the meteorological network to deﬁne an
average precipitation gradient perpendicular to the strike of the topography. This gradient
was then extrapolated parallel to strike across the study area. For each river segment
$500 m long, channel gradients (S) were extracted from the DEM, and discharge (Q)was
calculated as the product of upstream area and rainfall. Discharge is overestimated because
all rainfall is assumed to enter channels. Channel width (W) is calculated as 10
Speciﬁc stream power (in GJ m
) is calculated as r
QS/W, where r
is the density of
water and g is gravitational acceleration. Channel gradients and speciﬁc stream power are
binned every 5 km.
Received 20 June; accepted 4 November 2003; doi:10.1038/nature02187.
1. Koons, P. O. The topographic evolution of collisional mountain belts: A numerical look at the
Southern Alps, New Zealand. Am. J. Sci. 289, 1041–1069 (1989).
2. Beaumont, C., Jamieson, R. A., Nguyen, M. H. & Lee, B. Himalayan tectonics explained by extrusion
of a low-viscosity crustal channel coupled to focused surface denudation. Nature 414, 738–742 (2001).
3. Willett, S. D. Orogeny and orography: The effects of erosion on the structure of mountain belts.
J. Geophys. Res. 104, 28957–28982 (1999).
4. Hodges, K. V. Tectonics of the Himalaya and southern Tibet from two perspectives. Geol. Soc. Am.
Bull. 112, 324–350 (2000).
5. Tapponnier, P. et al. Oblique stepwise rise and growth of the Tibetan Plateau. Science 394, 1671–1677
6. Burchﬁel, B. D. et al. The South Tibetan detachment system, Himalayan orogen: Extension
contemporaneous with and parallel to shortening in a collisional mountain belt. Geol. Soc. Am. Spec.
Pap. 269, 1–41 (1992).
7. Harrison, T. M. et al. A late Miocene-Pliocene origin for the central Himalayan inverted
metamorphism. Earth Planet. Sci. Lett. 146, E1–E7 (1997).
8. Catlos, E. J. et al. Geochronologic and thermobarometric constraints on the evolution of the Main
Central Thrust, central Nepal Himalaya. J. Geophys. Res. 106, 16177–16204 (2001).
9. Robinson, D. M. et al. Kinematic model for the Main Central thrust in Nepal. Geology 31, 359–362
10. Hurtado, J. M. Jr, Hodges, K. V. & Whipple, K. Neotectonics of the Thakkhola Graben and
implications for Recent activity on the South Tibetan fault system in the central Nepal Himalaya. Geol.
Soc. Am. Bull. 113, 222–240 (2001).
11. Dodson, M. H. in Lectures in Isotope Geology (eds Jaeger, E. & Hunziker, C. J.) 194–202 (Springer, New
we, K., White, L. & Brown, R. The inﬂuence of eroding topography on steady-state isotherms.
Application to ﬁssion track analysis. Earth Planet. Sci. Lett. 124, 63–74 (1994).
13. Willett, S. D. & Brandon, M. T. On steady states in mountain belts. Geology 30, 175–178 (2002).
14. Zeitler, P. K. Cooling history of the NW Himalaya, Pakistan. Tectonics 4, 127–151 (1985).
15. Tippett, J. M. & Kamp, P. J. J. Fission track analysis of the Late Cenozoic vertical kinematics of
continental Paciﬁc crust, South Island, New Zealand. J. Geophys. Res. 98, 16119–16148 (1993).
16. Porter, S. C. Some geological implication of average Quaternary glacial conditions. Quat. Res. 32,
17. Ehlers, T. A., Armstrong, P. A. & Chapman, D. S. Normal fault thermal regimes and the interpretation
of low-temperature thermochronometers. Phys. Earth Planet. Inter. 126, 179–194 (2001).
18. Fort, M. B. Glacial extension and catastrophic dynamics along the Annapurna Front, Nepal Himalaya.
ttinger Geogr. Abh. 81, 105–121 (1986).
19. Duncan, C. C., Klein, A. J., Masek, J. G. & Isacks, B. L. Comparison of Late Pleistocene and modern
glacier extents in central Nepal based on digital elevation data and satellite imagery. Quat. Res. 49,
20. Hallet, B., Hunter, L. & Bogen, J. Rates of erosion and sediment evacuation by glaciers: A review of
ﬁeld data and their implications. Glob. Planet. Change 12, 213–235 (1996).
21. Hodges, K. V., Parrish, R. R. & Searle, M. P. Tectonic evolution of the central Annapurna Range,
Nepalese Himalayas. Tectonics 15, 1264–1291 (1996).
22. Burbank, D. W. et al. Bedrock incision, rock uplift, and threshold hillslopes in the northwestern
Himalaya. Nature 379, 505–510 (1996).
23. Whipple, K. E., Kirby, E. & Brocklehurst, S. H. Geomorphic limits to climate-induced increases in
topographic relief. Nature 401, 39–43 (1999).
24. Sklar, L. & Dietrich, W. E. Sediment supply, grain size and rock strength controls on rates of river
incision into bedrock. Geology 29, 1087–1090 (2001).
25. Wang, Q. et al. Present-day crustal deformation in China constrained by Global Positioning System
measurements. Science 294, 574–577 (2001).
26. Willett, S. D., Slingerland, R. & Hovius, N. Uplift, shortening, and steady state topography in active
mountain belts. Am. J. Sci. 301, 455–485 (2001).
27. Seeber, L. & Gornitz, V. River proﬁles along the Himalayan arc as indicators of active tectonics.
Tectonophysics 92, 335–367 (1983).
28. Pandey, M. R., Tandukar, R. P., Avouac, J. P., Lave, J. & Massot, J. P. Interseismic strain accumulation
on the Himalayan crustal ramp (Nepal). Geophys. Res. Lett. 22, 751–754 (1995).
Acknowledgements This work beneﬁted from discussions with K. Hodges, J. Lave
, A. Heimsath,
K. Whipple, P. Koons, M. Brandon and T. Ehlers. We thank P. Molnar and C. Beaumont for
comments and suggestions. Logistical support from Himalayan Experience and the Nepalese
Department of Hydrology and Meteorology is gratefully acknowledged. This work was funded by
the NSF Continental Dynamics program and by NASA.
Competing interests statement The authors declare that they have no competing ﬁnancial
Correspondence and requests for materials should be addressed to D.W.B.
consequences of trophy hunting
David W. Coltman
, Paul O’Donoghue
, Jon T. Jorgenson
, John T. Hogg
& Marco Festa-Bianchet
Department of Animal and Plant Sciences, University of Shefﬁeld,
Shefﬁeld S10 2TN, UK
Alberta Department of Sustainable Development, Fish and Wildlife Division,
Box 1059, Canmore, Alberta T0L 0M0, Canada
Montana Conservation Science Institute, Missoula, Montana 59803, USA
Department of Biological Sciences, University of Alberta, Edmonton,
Alberta T6G 2E9, Canada
partement de biologie, Universite
de Sherbrooke, Sherbrooke, Que
bec J1K 2R1,
Phenotype-based selective harvests, including trophy hunting,
can have important implications for sustainable wildlife manage-
ment if they target heritable traits
. Here we show that in an
evolutionary response to sport hunting of bighorn trophy rams
(Ovis canadensis) body weight and horn size have declined
signiﬁcantly over time. We used quantitative genetic analyses,
based on a partly genetically reconstructed pedigree from a
30-year study of a wild population in which trophy hunting
targeted rams with rapidly growing horns
evolutionary response to hunter selection on ram weight and
horn size. Both traits were highly heritable, and trophy-harvested
rams were of signiﬁcantly higher genetic ‘breeding value’ for
weight and horn size than rams that were not harvested. Rams of
letters to nature
NATURE |VOL 426 | 11 DECEMBER 2003 | www.nature.com/nature 655
high breeding value were also shot at an early age, and thus did
not achieve high reproductive success
. Declines in mean breed-
ing values for weight and horn size therefore occurred in
response to unrestricted trophy hunting, resulting in the pro-
duction of smaller-horned, lighter rams, and fewer trophies.
Sport harvesting is one of the most pervasive and potentially
intrusive human activities that affect game mammal populations
. Hunters are willing to pay large sums to hunt trophy
mountain ungulates in various parts of the world, and many
mountain sheep (Ovis canadensis and O. dalli) populations in
North America are managed primarily to produce large-horned
trophy rams for sport hunters. A world-class trophy ram is an
extremely valuable commodity, and hunting permits have been
auctioned for hundreds of thousands of dollars
. One sport hunter
paid over Can$1 million in 1998 and 1999 for special permits to
hunt trophy rams in Alberta, Canada
. In many parts of North
America, sport harvest of mountain sheep is often restricted only
by the availability of rams whose horns reach a minimum size
prescribed by regulations. Although the use of income generated
from sport hunting towards enhancing and conserving mountain
ungulate habitat can be seen in a positive light
, so far little attention
has been paid to the potential evolutionary consequences, and
hence the sustainability, of harvest regimes
Wildlife management has traditionally focused on demographic
and ecological factors that affect numbers and growth rates in
. However, the life-history changes experi-
enced by species subject to commercial ﬁsheries strongly suggest
that intensive harvesting practices can elicit an evolutionary
response in wild stocks
. Experimental size-selective harvesting
treatments on an exploited ﬁsh demonstrated evolutionary effects
on somatic growth and population productivity in the opposite
direction of the size bias of the harvest
. Recent reviews have called
attention to the potential selective effects of sport hunting on wild
ungulates, in which large-horned or large-antlered males are selec-
. The increased frequency of tuskless elephants in
many African populations has also been suggested to have occurred
in response to selective ivory poaching
. Here we use data from the
long-term study of a harvested bighorn sheep population at Ram
Mountain, Alberta, Canada, to investigate the evolutionary con-
sequences of more than 30 years of selective hunting of trophy rams.
Fifty-seven rams have been shot at Ram Mountain since 1975, or
about 40% of the rams legally available for harvest in each year (see
Methods), for a yearly harvest of between zero and six rams
trophy-harvested rams were shot before reaching 8 years of age (45
of 57 rams), and nine were shot as early as the age of 4 years. In
bighorn sheep, much of the total horn length is added from the ages
of 2 to 4 years, and at Ram Mountain the probability of a ram being
shot before the age of 6 years is positively correlated with cumulative
horn growth over this interval
. ‘Animal model’
genetic analysis of 395 horn-length and 447 weight measurements
taken from 192 rams at ages 2, 3 and 4 years from 1971 to 2002
revealed narrow-sense heritabilities of 0.69 ^ 0.10 and 0.41 ^ 0.11
Figure 1 Selection against high-breeding-value rams imposed by trophy hunting.
a, Breeding values (means ^ s.e.m.) for horn length and weight of trophy-harvested
rams (ﬁlled bars) and non-trophy-harvested rams (open bars). b, Relationship between
the age at harvest for trophy-harvested rams and their breeding value. c, Relationship
between the number of paternities assigned to trophy-harvested rams in their lifetime and
their breeding value.
Figure 2 Observed changes in mean weight and horn length and in the population size
from 1972 to 2002. a, Relationship between weight (mean ^ s.e.m.) of 4-year-old rams
and year (N ¼ 133 rams). b, Relationship between horn length (mean ^ s.e.m.) of
4-year-old rams and year (N ¼ 119 rams). c, Changes in population size (taken as the
number of ewes aged at least 2 years plus yearlings
) over time.
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NATURE | VOL 426 | 11 DECEMBER 2003 | www.nature.com/nature656
(means ^ s.e.m.), respectively (see Methods), and a strong positive
additive genetic correlation between the two (þ0.84 ^ 0.10). Com-
parison of expected genetic ‘breeding values’ (twice the expected
deviation of an individual’s offspring phenotype from the popu-
lation mean owing to the additive effect of the offspring’s inherited
) extracted from this model (Fig. 1a) indicates that hunters
selectively harvest rams with high breeding values for horn length
(trophy-harvested mean, þ 0.61 ^ 0.28; non-harvested mean,
21.24 ^ 0.48; t-test: t
¼ 24.16, P , 0.001) and weight (tro-
phy-harvested mean, þ0.70 ^ 0.28; non-harvested mean,
20.89 ^ 0.48; t-test: t
¼ 23.26, P ¼ 0.0014).
Within seasons, mating success in bighorn sheep increases with
, age and horn length
. The positive effect of large
horns on mating success increases from about 6 years of age
rams are capable of defending oestrous ewes during the rut. The age
at which a high-breeding-value ram is harvested is therefore likely to
have an important impact on the number of offspring he can sire.
We found a negative relationship between the age at which a trophy-
harvested ram was shot and his breeding value for horn length
(generalized linear model (GLM) with Poisson errors: x
P ¼ 0.031; Fig. 1b) but not for weight (GLM: x
¼ 1.80, P ¼ 0.18;
data not shown). Trophy-harvested rams with high breeding values
for body and horn size were therefore less likely to reach the ages at
which they achieve high rates of paternity in this population
consequence, there was a negative relationship between breeding
value for horn length and lifetime mating success, measured as the
number of paternities assigned over their lifetime, among trophy-
harvested rams (GLM with negative binomial error: x
P ¼ 0.0034; Fig. 1c). The mean sire breeding value of individuals
fathered by trophy-harvested rams was therefore signiﬁcantly less
than zero for both weight (one-sample t-test: mean ¼ 22.41,
s.e.m. ¼ 0.37, t
¼ 26.50, P , 0.001) and horn length
(mean ¼ 21.84, s.e.m. ¼ 0.19, t
¼ 29.68, P , 0.001). The
mean sire breeding value of individuals fathered by rams that
died a natural death was also signiﬁcantly less than zero for both
weight (one-sample t-test: mean ¼ 21.24, s.e.m. ¼ 0.17,
¼ 27.14, P , 0.001) and horn length (mean ¼ 22.10,
s.e.m. ¼ 0.16, t
¼ 220.43, P , 0.001). The low breeding values
of rams not harvested (Fig. 1a) and the reduced longevity and
potential reproductive output of the higher-quality trophy-har-
vested rams (Fig. 1b, c) combine to suggest that the selection
imposed by trophy hunting had a negative impact on the evol-
utionary trajectory of horn length and body weight in this popu-
lation during our study.
Is there evidence of a response to selective harvesting at the
population level? Signiﬁcant declines in both ram weight (linear
mixed-effect model including year of birth and individual as a
random effects, and age, time and resource index as ﬁxed effects:
¼ 20.30, s.e.m. ¼ 0.09, t
¼ 23.42, P ¼ 0.0021) and horn
length (linear mixed-effect model including year of birth and
individual as a random effects, and age, time and resource index
as ﬁxed effects: b
¼ 20.35, s.e.m. ¼ 0.12, t
P ¼ 0.0068) were observed over the course of the study (Fig. 2a,
b) after controlling for environmental effects such as population
density (Fig. 2c) using an index of resource availability (see
Methods; weight: b
¼ 0.81, s.e.m. ¼ 0.17, t
P , 0.001; horn length: b
¼ 0.72, s.e.m. ¼ 0.22,
¼ 3.32, P ¼ 0.0030). These are very rapid rates of phenotypic
,correspondingto20.30/12.9 ¼ 20.023 and 20.35/
13.6 ¼ 20.026 standard deviations per year, or 20.14 and 20.15
haldanes (ref. 20) assuming a generation time of 6 years. Analyses of
breeding values are consistent with genetically based responses (Fig.
3). Declines in breeding value (see Methods) were observed for both
ram weight (linear mixed-effect model including year of birth as a
random effect, and time and resource index as ﬁxed effects:
¼ 0.037, s.e.m. ¼ 0.025, t
¼ 1.49, P ¼ 0.15;
¼ 20.071, s.e.m. ¼ 0.012, t
¼ 26.02, P , 0.001) and
horn length (linear mixed-effect model including year of birth as
a random effect, and time and resource index as ﬁxed effects:
¼ 0.050, s.e.m. ¼ 0.024, t
¼ 2.08, P ¼ 0.045;
¼ 20.075, s.e.m. ¼ 0.011, t
2 6.76, P , 0.001). Such
declines in breeding value over time are indicative of a microevolu-
tionary response to selection
in the Ram Mountain population.
Unrestricted harvesting of trophy rams has thus contributed to a
decline in the very traits that determine trophy quality. Hunters
have selectively targeted rams of high genetic quality before their
reproductive peak, depleting the genes that confer rapid early body
and horn growth. Wildlife harvesting that is selective and sufﬁ-
ciently severe might elicit an undesired evolutionary response when
the target trait is heritable. There might also be unexpected effects
on genetically correlated traits, such as female body weight or
, that could result in further genetic deterioration
of harvested populations as anthropogenic selection pushes traits
away from their naturally selected optima. Because such changes
will be extremely difﬁcult to reverse, wildlife managers must
consider the genetic effects and the evolutionary implications of
alternative harvest strategies
. The move to adopt a ‘full curl’
restriction in parts of Alberta in 1996, which limits harvest to
rams with horns whose tip extends beyond the tip of the nose, is one
strategy to minimize further deterioration of the genetic quality of
bighorn sheep. A
Population and study site
The bighorn sheep population on Ram Mountain, Alberta, Canada (528 N, 1158 W,
elevation 1,080–2,170 m) has been monitored closely since 1971 (refs 17, 23). Immigration
to Ram Mountain from the main species range has not been documented, and is probably
rare because of isolation of the population by about 30 km of coniferous forest. Each year,
sheep were captured in a corral trap baited with salt from late May to early October, and
marked with coloured plastic ear tags or canvas collars for individual identiﬁcation. Adult
rams were captured once or twice in most summers from early June to mid-July. At each
capture, sheep were weighed to the nearest 250 g with a Detecto spring scale. Horn length
along the outside curvature was measured with tape. The longer of the left and right horn
measurements was used, because rams can have a varying amount of horn removed by
wear. For further details on ﬁeld methods see refs 17, 23 and 24.
Bighorn males on Ram Mountain can be legally harvested by Alberta resident hunters
from late August to the end of October. Until 1996, rams with horns describing at least
four-ﬁfths of a curl (‘trophy’ rams) could be harvested by any hunter holding a trophy
. As any resident could purchase a licence, the harvest was limited only by
the availability of trophy rams. A change in regulations in 1996 limited harvest to ‘full-curl’
rams. Consequently, only three rams have been shot since 1996. Individual weight and
horn length measurements from rams captured between 1971 and 2002 were adjusted to
5 June (ref. 24). Because the youngest age at which rams were shot by hunters was 4 years,
we used weight and horn length data from ages 2, 3 and 4 years to avoid bias due to hunter
Maternity was known from ﬁeld observations for 709 of the 894 (79.3%) marked sheep
Figure 3 Changes in the mean breeding value of cohorts born between 1967 and 2002.
a, Relationship between breeding value (mean ^ s.e.m.) for weight and year of birth
(N ¼ 783 individuals). b, Relationship between breeding value (mean ^ s.e.m.) for horn
length and year of birth (N ¼ 783 individuals).
letters to nature
NATURE |VOL 426 | 11 DECEMBER 2003 | www.nature.com/nature 657
whose fates have been followed since 1971. Tissue sampling for DNA analyses started in
1988. Blood samples were taken from all captured sheep until 1993 and stored in
preservative at 220 8C. Sampling resumed in 1997, when hair samples were taken from all
captured sheep by plucking 50–100 hairs including roots from the back or ﬂank. Hairs
were kept either in paper envelopes or plastic bags containing about 5 g of silica at room
temperature. From 1998 to 2002, a tissue sample from each captured sheep was taken from
the ear with an 8-mm punch. Ear tissue was kept at 220 8C in a solution of 20%
dimethylsulphoxide saturated with NaCl. We sampled 433 marked individuals over the
course of the study.
DNAwas extracted from blood with a standard phenol–chloroform method, and from
either 20–30 hairs including follicles or about 5 mg of ear tissue, using the QIAamp tissue
extraction kit (Qiagen Inc., Mississauga, Ontario). Polymerase chain reaction
ampliﬁcation at 20 ungulate-derived microsatellite loci, 15 as described previously
MCM527, BM4025, MAF64, OarFCB193 and MAF92 (refs 25, 26), and fragment analysis
were performed as described elsewhere
. After correction for multiple comparisons, we
found no evidence for allelic or genotypic disequilibria at or among these 20 loci.
Paternity of 241 individuals was assigned by using the likelihood-based approach
described in CERVUS
at a conﬁdence level of more than 95% with input parameters
given in ref. 5. After paternity analysis, we used KINSHIP
to identify 31 clusters of 104
paternal half-sibs among the unassigned offspring. A paternal half-sibship consisted of all
pairs of individuals of unassigned paternity that were identiﬁed in the KINSHIP analysis as
having a likelihood ratio of the probability of a paternal half-sib relationship versus
unrelated with an associated P , 0.05 (ref. 28). Members of reconstructed paternal half-
sibships were assigned a common unknown paternal identity for the animal model
analyses. Paternal identity links in the pedigree were therefore deﬁned for 345 individuals.
Animal model analyses
Breeding values, genetic variance components and heritabilities were estimated by using a
multiple trait restricted-estimate maximum-likelihood (REML) model implemented by
the programs PEST
. An animal model was ﬁtted in which the phenotype of
each animal was broken down into components of additive genetic value and other
random and ﬁxed effects: y ¼ Xb þ Za þ Pc þ e, where y was a vector of phenotypic
values, b was a vector of ﬁxed effects, a and c were vectors of additive genetic and
permanent environmental, e was a vector of residual values, and X, Z and P were the
corresponding design matrices relating records to the appropriate ﬁxed or random
. Fixed effects included age (factor) and the average weight of yearling ewes in the
year of measurement (covariate), which is a better index of resource availability than
population size because it accounts for time-lagged effects
. The permanent
environmental effect grouped repeated observations on the same individual to quantify
any remaining between-individual variance over and above that due to additive genetic
effects, which would be due to maternal or other long-term environmental and non-
additive genetic effects.
The total phenotypic variance (V
) was therefore partitioned into three components:
the additive genetic variance (V
), the permanent environmental variance (V
) and the
residual variance (V
), thus: V
. Heritability was calculated as h
. The VCE
program returns standard errors on all variance components and ratios.
Best linear unbiased predictors of individual breeding values were quantiﬁed by using
REML estimates of the variance components obtained with PEST
. All statistical tests
were conducted in SPLUS 6.1.
Received 11 August; accepted 17 October 2003; doi:10.1038/nature02177.
1. Thelen, T. H. Effects of harvest on antlers of simulated populations of elk. J. Wild. Mgmt 55, 243–249
2. Harris, R. B., Wall, W. A. & Allendorf, F. W. Genetic consequences of hunting: what do we know and
what should we do? Wildl. Soc. Bull. 30, 634–643 (2002).
3. Festa-Bianchet, M. in Animal Behavior and Wildlife Conservation (eds Apollonio, M. &
Festa-Bianchet, M.) 191–207 (Island Press, Washington DC, 2003).
4. Festa-Bianchet, M., Coltman, D. W., Turelli, L. & Jorgenson, J. T. Relative allocation to horn and body
growth in bighorn rams varies with resource availability. Behav. Ecol. (in the press).
5. Coltman, D. W., Festa-Bianchet, M., Jorgenson, J. T. & Strobeck, C. Age-dependent sexual selection in
bighorn rams. Proc. R. Soc. Lond. B 269, 165–172 (2002).
6. Milner-Gulland, E. J. et al. Conservation
reproductive collapse in saiga antelope harems. Nature 422,
7. Marty, S. Sacriﬁcial ram. Can. Geographic November/December, 37–50 (2002).
8. Clutton-Brock, T. H., Coulson, T. N., Milner-Gulland, E. J., Thomson, D. & Armstrong, H. M. Sex
differences in emigration and mortality affect optimal management of deer populations. Nature 415,
9. Ginsberg, J. R. & Milner Gulland, E. J. Sex-biased harvesting and population dynamics in ungulates
implications for conservation and sustainable use. Conserv. Biol. 8, 157–166 (1994).
10. Langvatn, R. & Loison, A. Consequences of harvesting on age structure, sex ratio and population
dynamics of red deer Cervus elaphus in central Norway. Wildl. Biol. 5, 213–223 (1999).
11. Laurian, C., Ouellet, J. P., Courtois, R., Breton, L. & St-Onge, S. Effects of intensive harvesting on
moose reproduction. J. Appl. Ecol. 37, 515–531 (2000).
12. Ashley, M. V. et al. Evolutionarily enlightened management. Biol. Conserv. 111, 115–123 (2003).
13. Conover, D. O. & Munch, S. B. Sustaining ﬁsheries yields over evolutionary time scales. Science 297,
14. Palumbi, S. R. Evolution
humans as the world’s greatest evolutionary force. Science 293, 1786–1790
15. Law, R. Fishing, selection, and phenotypic evolution. Ices J. Mar. Sci. 57, 659–668 (2000).
16. Jachmann, H., Berry, P. S. M. & Imae, H. Tusklessness in African elephants
a future trend. Afr. J. Ecol.
33, 230–235 (1995).
17. Jorgenson, J. T., Festa-Bianchet, M. & Wishart, W. D. Effects of population density on horn
development in bighorn rams. J. Wildl. Mgmt 62, 1011–1020 (1998).
18. Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Massachusetts, Sinauer,
19. Hogg, J. T. & Forbes, S. H. Mating in bighorn sheep: frequent male reproduction via a high-risk
‘unconventional’ tactic. Behav. Ecol. Sociobiol. 41, 33–48 (1997).
20. Hendry, A. P. & Kinnison, M. T. Perspective: The pace of modern life: measuring rates of
contemporary microevolution. Evolution 53, 1637–1653 (1999).
, J., Kruuk, L. E. B. & Sheldon, B. C. Cryptic evolution in a wild bird population. Nature 412,
22. Coltman, D. W., Pilkington, J., Kruuk, L. E. B., Wilson, K. & Pemberton, J. M. Positive genetic
correlation between parasite resistance and body size in a free-living ungulate population. Evolution
55, 2116–2125 (2001).
23. Jorgenson, J. T., Festa-Bianchet, M. & Wishart, W. D. Harvesting bighorn ewes
population-size and trophy ram production. J. Wildl. Mgmt 57, 429–435 (1993).
24. Festa-Bianchet, M., Jorgenson, J. T., King, W. J., Smith, K. G. & Wishart, W. D. The development of
sexual dimorphism: seasonal and lifetime mass changes in bighorn sheep. Can. J. Zool. 74, 330–342
25. Crawford, A. M. et al. An autosomal genetic linkage map of the sheep genome. Genetics 140, 703–724
26. Slate, J. et al. Bovine microsatellite loci are highly conserved in red deer (Cervus elaphus), sika deer
(Cervus nippon) and Soay sheep (Ovis aries). Anim. Genet. 29, 307–315 (1998).
27. Marshall, T. C., Slate, J., Kruuk, L. E. B. & Pemberton, J. M. Statistical conﬁdence for likelihood-based
paternity inference in natural populations. Mol. Ecol. 7, 639–655 (1998).
28. Goodnight, K. F. & Queller, D. C. Computer software for performing likelihood tests of pedigree
relationship using genetic markers. Mol. Ecol. 8, 1231–1234 (1999).
29. Groeneveld, E., Kovac, M., Wang, T. L. & Fernando, R. L. Computing algorithms in a general purpose
BLUP package for multivariate prediction and estimation. Arch. Anim. Breed. 15, 399–412 (1992).
30. Groeneveld, E. User’s Guide: REML VCE, a Multivariate Multi-Model Restricted Maximum Likelihood
(Co)variance Estimation Package, Version 3.2 (Institute of Animal Husbandry and Animal Behaviour,
Federal Research Center of Agriculture (FAL) (Mariensee, Germany, 1995).
Acknowledgements We thank the many students, colleagues, volunteers and assistants that
contributed to this research over the past 30 years.B. Wishart initiated the Ram Mountain project.
Our research was funded by the Alberta Conservation Association, Alberta Fish and Wildlife
Division, Alberta Recreation, Sports, Parks and Wildlife Foundation, Eppley Foundation for
Research, Foundation for North American Wild Sheep, National Geographic Society, Natural
Environment Research Council (UK), Natural Sciences and Engineering Research Council of
Canada, Rocky Mountain Elk Foundation (Canada), and the Universite
de Sherbrooke. We are
grateful for the logistical support of the Alberta Forest Service.
Competing interests statement The authors declare that they have no competing ﬁnancial
Correspondence and requests for materials should be addressed to D.W.C.
emergence of infectious diseases
, Roland R. Regoes
, Jacob C. Koella
& Carl T. Bergstrom
Department of Biology, Emory University, Atlanta, Georgia 30322, USA
Laboratoire de Parasitologie Evolutive, Universite
Pierre et Marie Curie,
75252 Paris, France
Department of Biology, University of Washington, Seattle, Washington 98195,
It is unclear when, where and how novel pathogens such as
human immunodeﬁciency virus (HIV), monkeypox and severe
acute respiratory syndrome (SARS) will cross the barriers that
separate their natural reservoirs from human populations and
ignite the epidemic spread of novel infectious diseases. New
pathogens are believed to emerge from animal reservoirs when
ecological changes increase the pathogen’s opportunities to enter
the human population
and to generate subsequent human-to-
. Effective human-to-human transmission
requires that the pathogen’s basic reproductive number, R
should exceed one, where R
is the average number of secondary
infections arising from one infected individual in a completely
. However, an increase in R
, even when
insufﬁcient to generate an epidemic, nonetheless increases the
number of subsequently infected individuals. Here we show that,
letters to nature
NATURE | VOL 426 | 11 DECEMBER 2003 | www.nature.com/nature658