Download Necksforsex or competing browsers? A critique of ideas on the

Journal of Zoology
Journal of Zoology. Print ISSN 0952-8369
Necks-for-sex or competing browsers? A critique of ideas
on the evolution of giraffe
R. E. Simmons1 & R. Altwegg2,3
1 DST/NRF Centre of Excellence at the Percy FitzPatrick Institute, University of Cape Town, Rondebosch, South Africa
2 South African National Biodiversity Institute, Kirstenbosch Research Centre, Claremont, South Africa
3 Animal Demography Unit, University of Cape Town, Department of Zoology, Rondebosch, South Africa
Keywords
sexual selection; ancestral giraffids;
competing browsers; necks-for-sex; female
choice; allometry.
Correspondence
DST/NRF Centre of Excellence at the Percy
FitzPatrick Institute, University of Cape
Town, Rondebosch 7701, South Africa.
Email: [email protected]
Editor: Nigel Bennett
Received 4 December 2009; revised 23
March 2010; accepted 23 March 2010
doi:10.1111/j.1469-7998.2010.00711.x
Abstract
Recent years have witnessed a resurgence in tests of the evolution and origin of the
great height and long neck of the giraffe Giraffa camelopardalis. The two main
hypotheses are (1) long necks evolved through competition with other browsers
allowing giraffe to feed above them (‘competing browsers’ hypothesis); or (2) the
necks evolved for direct use in intra-sexual combat to gain access to oestrous
females (‘necks-for-sex’ hypothesis). Here, we review recent developments and
their relative contribution in explaining giraffe evolution. Trends from Zimbabwean giraffes show positive allometry for male necks and isometry for female
necks relative to body mass, while comparative analyses of the cervical versus the
total vertebral column of the giraffe, okapi and fossil giraffe suggest selection
specifically on neck length rather than on overall height. Both support the necksfor-sex idea. Neither study, however, allows us to refute one of the two ideas. We
suggest new approaches for quantifying the relative importance of the two
hypotheses. A direct analysis of selection pressure on neck length via survival and
reproduction should clarify the mechanism maintaining the trait, while we predict
that short robust ossicones should have arisen concurrently with incipient neck
elongation if sexual selection was the main selective driver. The main challenge for
the competing browser hypothesis is to explain why giraffe have remained about
2 m taller than their tallest competitors for over 1 Myr, whereas the sexual selection
hypothesis cannot provide an adaptive explanation for the long neck of female
giraffe. We conclude that probably both mechanisms have contributed to the
evolution and maintenance of the long neck, and their relative importance can be
clarified further.
New data and tests of the origin of the elongated neck of the
giraffe Giraffa camelopardalis have provided fresh insight
into the origin of this trait. All attempt to test one of two
main hypotheses – that of natural selection via advantages
from feeding on trees above competitors (Darwin, 1871) or
intra-sexual (male–male) competition via advantages found
in clubbing rivals more effectively in competition for
females (Simmons & Scheepers, 1996). Both mechanisms
should result in longer necks and both are demonstrably
advantageous to their bearers (Pratt & Anderson, 1982,
1985; Cameron & du Toit, 2007). Although both mechanisms can explain long necks in giraffes, no tests have
attempted to distinguish between them as the origin or
maintenance of the long neck. The two hypotheses may
not be mutually exclusive, and it may not be possible to
differentiate between them if both have provided selective
pressures to neck lengthening. The question, therefore,
should be what is the relative importance of the two
6
mechanisms in explaining the origin and maintenance of
the giraffe’s long neck?
Here, we review and clarify the main hypotheses, explore
the tests that have been advanced and provide future tests
for prising them apart.
Evolution of the long necks: main
hypotheses
The ‘competing browsers’ idea, elucidated by later editions
of Darwin (1871) proposed that the competition between
browsing species for access to leaves from tall trees created
an advantage for giraffe to out-reach their tallest rivals
(Darwin, 1871). The individuals doing so survive food
bottlenecks during dry-season dearths and live to pass on
their long-necked genes to future generations. Observing
giraffes browse from 5-m-tall Acacia suggests that the idea is
secure with little need for further debate. However,
c 2010 The Authors. Journal compilation c 2010 The Zoological Society of London
Journal of Zoology 282 (2010) 6–12 R. E. Simmons and R. Altwegg
Simmons & Scheepers (1996) found inconsistent support
from foraging studies, and recent evidence (Shorrocks,
2009) also indicates that animals frequently feed at shoulder
level, during winter bottlenecks (Ginnett & Demment,
1997), when their neck should assist them in gaining a
feeding height advantage. The finding that giraffe feed faster
at shoulder level (2.5 m for females and 3.0 m for males) in
East Africa (Young & Isbell, 1991), and spend more time
doing so than at higher levels (Young & Isbell 1991; Ginnett
& Demment, 1997) also suggests patchy advantages from
elsewhere in Africa. That giraffe are considerably taller than
competing browsers and have been so for more than 1 Myr
(Mitchell & Skinner, 2003) suggests other selection pressures
at work on the neck. Can this be explained by competition
from other extant browsers such as elephant Loxodonta
africana and black rhino Diceros bicornis? Both species push
over trees or destroy them while feeding, especially in times
of drought (Smithers, 1983; Estes, 1991). This behaviour
suggests that height per se is not likely to confer much
advantage to a tall giraffe.
However, South African giraffe were found to browse
more often above shoulder level (du Toit, 1990), partly
because more browse was available there (Woolnough &
du Toit, 2001) and partly due to their move into dry
riverbeds in winter where leaves remained on tall trees (du
Toit, 1995). Further experimental support was found in an
elegant field study of feeding competition, indicating that
more forage was available above 2.5 m in fenced trees at
levels used by giraffe (relative to un-exclosed trees) because
of the competition with shorter browsers (Cameron & du
Toit, 2007). Their results support Darwin’s original hypothesis but do not distinguish between it and the sexual
selection alternative (Cameron & du Toit, 2007).
This so-called ‘necks-for-sex’ idea (Senter, 2007) suggested that long, powerful necks were sexually selected as
clubs, allowing males with large powerful necks to beat
rivals for access to oestrous females. Females don’t fight,
and so they are predicted to have less powerful necks.
Feeding competition predicts equally long necks if both
sexes benefit from feeding above other browsers. Clubbing
involves males standing flank to flank and head to head, and
smashing the back of the head into their opponents ribs and
legs by whipping the neck back and then towards their rival.
Fatalities are not uncommon (Simmons & Scheepers, 1996).
Female mate choice may also play a role if females prefer
males with larger necks.
Several lines of evidence support the sexual selection idea:
(1) males with larger necks win most contests for access to
oestrous females (Pratt & Anderson 1982, 1985); (2) oestrous females show preference for large-necked males or
darker, older males (Pratt & Anderson, 1985; Brand, 2007);
(3) dominance contests involve prominent displays of the
long neck by male giraffe during erect walking (Dagg &
Foster, 1976; Estes, 1991; Brand, 2007); (4) sexually selected
traits are condition-dependent and costly (Darwin, 1871;
Kodric-Brown & Brown, 1984; Andersson, 1994), for which
there is some support from sex-biased mortality and physiological costs . Morphologically (5) sexually selected traits are
Giraffid evolution revisited
usually positively allometric (Clutton-Brock, Albon, Harvey, 1980; Petrie, 1992; Kodric-Brown, Sibly, Brown, 2006),
relative to body size, a trait confirmed for giraffe necks and
heads (Simmons & Scheepers, 1996); and (6) the fossil
record should show a departure from typical ratios of neck
vertebrae to remaining vertebrae lengths, for extant giraffe
relative to ancestral giraffids, as confirmed by Badlangana,
Adams, Manger, (2009).
Testing between hypotheses: directly
observed selection pressure
The best evidence for either hypothesis would be directly
observed fitness benefits. The observation that largernecked male giraffes win contests more often than smallernecked giraffes and are preferred by oestrous females (Pratt
& Anderson 1982, 1985) provides direct evidence indicating
that sexual selection on neck size is occurring. Paternity tests
are required to confirm that these mating advantages lead to
higher reproductive success. We are unaware of similar
direct evidence for the feeding competition hypothesis (i.e.
taller giraffe survive food bottlenecks). Estimating sexspecific selection on neck characteristics in individually
recognizable giraffes would be a powerful tool for quantifying the selection pressure acting on the two sexes, and for
measuring short-term evolutionary change. This has been
done for other species (e.g. Roulin et al., 2010), and a study
of giraffe could largely settle the question regarding what
maintains the long neck. The feeding competition hypothesis predicts positive selection on both sexes, whereas the
sexual selection hypothesis predicts neutral selection on
females and positive selection on males. Differential food
resource allocation between male and female giraffe has
been well studied (Young & Isbell, 1991; Ginnett & Demment, 1997), but its role in reducing food competition
between the sexes remains unexplored; this too may influence natural selection on neck length.
Necks: size matters
Under sexual selection, males should have proportionally
larger necks and heads than females, whereas the competing
browsers idea predicts similar relationships for both sexes,
assuming no inter-sexual competition. Sexually selected
traits are more often positively allometric than naturally
selected ones among mammals (Kodric-Brown et al., 2006),
but not universally so (Bonduriansky, 2007; Cuervo &
Moller, 2009). Thus, positive allometry is more likely for
male giraffe under sexual selection than for females and this
was verified for 77 Namibian giraffe (Simmons & Scheepers,
1996). This hypothesis has been re-assessed recently using a
Zimbabwean sample (Mitchell, van Sittert, Skinner, 2009,
n = 17 males and 21 females). The allometric relationship is
given by
T ¼ aM k
ð1Þ
where T is the trait of interest (the neck mass or the head
mass in this case), M is the body mass (excluding the neck
c 2010 The Authors. Journal compilation c 2010 The Zoological Society of London
Journal of Zoology 282 (2010) 6–12 7
Giraffid evolution revisited
R. E. Simmons and R. Altwegg
and head mass to make T independent of M) and a is a
constant. The exponent k determines whether the relationship between T and the body mass is isometric (k1),
positively allometric (k 41) or negatively allometric (ko1).
The Zimbabwean studies fitted linear regression models
after taking the logarithm on both sides of equation (1). We
re-analysed the Namibian data using non-linear regression
models implemented in the function nls in program R 2.9.0
(R Development Core Team, 2009). The critical question is
whether k differs between the sexes, and this approach
allows us to test this statistically. We modified equation (1)
to include sex (s: 0 = male, 1 =female):
T = ða+bsÞM ðk+csÞ
ð2Þ
.Parameters b and c estimate sex differences in the constant
and in the exponent, respectively. Differences between the
Namibian and Zimbabwean data could be tested formally in
a similar way. Therefore, we requested the original data
from Mitchell and colleagues but our request was refused
(G. Mitchell, pers. comm.).
Results from Namibia were similar to that originally
reported (Simmons & Scheepers, 1996): neck mass showed
a positive allometric relationship to body mass in males
[Fig. 1; k= 1.34, 95% confidence interval (CI): 1.16–1.51]
and an isometric relationship in females (Fig. 1; k= 0.90, CI:
0.69–1.10). This difference was significant (parameter c in
equation (2) significantly different from zero, P= 0.007).
Slopes derived previously using RMA regression for males
(k= 1.35) and females (k= 0.97) were similar (Simmons &
Scheepers, 1996). Mitchell et al. (2009) reported k=1.13 for
males and k= 1.06 for females in their smaller Zimbabwean
sample. While Mitchell et al. (2009) interpreted their results
120
Females
Males
Neckmass (kg)
100
80
60
40
20
as evidence for positive allometry in both sexes, they reported
neither confidence intervals or significance levels for k nor
differences between the sexes. The k= 1.06 reported for
Zimbabwean females (Mitchell et al., 2009) appears to reveal
isometry, not positive allometry, because it lies close to 1.00
and within confidence limits from the Namibian dataset; thus
the two populations probably do not differ significantly.
Mitchell et al. (2009) appear to have misinterpreted this
result, and their data therefore support the idea that female
neck mass is directly related to body size, a pattern not
usually seen in sexually selected traits.
Mitchell et al. (2009) also measured neck length and
found no apparent difference in dimensions between males
and females (significance levels were unreported) or in neck
length regressed against body mass for males and females.
However, sexual selection does not directly predict allometrically longer necks but more powerful ones for males.
Female’s necks could be equally long but ineffective as clubs
because clubbing combines neck length and neck size
(related to muscle mass) to generate momentum in the head
for clubbing rivals (Simmons & Scheepers, 1996; Simmons,
2008). Differentiating the muscle to bone components in the
neck (Mitchell et al., 2009) indeed shows that the mass
difference is due to muscle mass and not due to bone density.
While Dagg & Foster (1976) indicate that necks of females
are about 35 cm shorter, data presented on neck length by
Mitchell et al. (2009) indicated that ‘females were 18.3 cm
shorter, but with necks 4.6 cm longer and forelegs 2.6 cm
longer than males of the same mass’. This suggests some
discrepancy in their measurements but again original data
were unavailable. The critical point is that males need only a
long neck to reach high-level leaves (natural selection
hypothesis), not a massive and ever increasing one to do so.
For sexual selection, this is required and predicted for males
and not for females. Thus, both Zimbabwean and Namibian
data support the sexual selection idea on male necks.
Furthermore, the neck mass of male but not female giraffe
in the Namibian sample continued to increase with age, as
expected for a trait that enhances intra-sexual combat.
Growth in relation to age of Zimbabwean giraffes was not
given.
Sexual selection of size and shape in ungulates is, of
course, not limited to giraffe and it may well explain the
dimorphism of many species, including a larger body size
and the growth of male characters such as horns and antlers
(e.g. Bergeron et al., 2008). These in turn can be reliable
indicators of mating success or individual fitness-related
traits (Malo et al., 2005; Vanpe et al., 2007).
Heads as clubs
200
400
600
800
Body mass (kg)
1000
1200
Figure 1 Neck mass of a sample of Namibian female (n = 43) and male
(n =34) giraffe Giraffa camelopardalis, in relation to their body mass.
Body mass here excludes the mass of the neck and the head. The
fitted non-linear regression lines are shown and are significantly
different. R2 of the fitted model was 0.89.
8
If sexual selection contributed to the evolution of giraffes’
large neck for clubbing opponents, we expect significant
differences between the sexes in head mass. Conversely, if
feeding competition was the sole selective force, no differences would be expected. Re-evaluating the Namibian data
(Simmons & Scheepers, 1996) using the allometric methods
described above indicated that males had significantly
c 2010 The Authors. Journal compilation c 2010 The Zoological Society of London
Journal of Zoology 282 (2010) 6–12 R. E. Simmons and R. Altwegg
Giraffid evolution revisited
35
Females
Males
Headmass (kg)
30
25
20
15
10
5
200
400
600
800
Body mass (kg)
1000
1200
Figure 2 Head mass of a sample of Namibian female (n = 43) and male
(n = 35) giraffe Giraffa camelopardalis, in relation to their body mass.
Body mass here excludes the mass of the neck and the head. The
fitted non-linear regression lines are shown and are significantly
different. R2 of the fitted model was 0.88.
steeper allometric slopes than females (Fig. 2; males
k = 0.96, CI: 0.83–1.09, and females k = 0.73, CI:
0.56–0.90). These relationships were isometric for males
and negatively allometric for females, and the differences
were significant (P= 0.049).
The Zimbabwean data showed similar trends with both
estimates contained in the confidence intervals for the
Namibian estimates (males k = 0.87, females k = 0.80:
Mitchell et al. 2009).
Males, but not females, in Namibia also continue to
invest in heavier heads as they age (Simmons & Scheepers,
1996) and this is corroborated by independent museum data
(Seymour, 2001). For same-length skulls, male giraffe skulls
from all subspecies were up to fourfold heavier than that of
females (mean for males x =8.23 kg, n = 90; females
x = 2.19 kg, n = 40: Seymour, 2001). While both sexes continued growing heavier, males did so much more by depositing superficial bone over the skull to reach masses up
to 14.8 kg (compared with 3.0 kg for females: Seymour,
2001). Age-related growth from Zimbabwe giraffe were
unreported.
Additional tests of natural and sexual
selection ideas: costs and physiology
Morphology is but one line of evidence separating the two
hypotheses. Others include patterns of gender-specific costs,
and the fossil record that can provide qualitative data on
neck length (in relation to leg lengths) in fossil giraffids.
As giraffid necks lengthened through evolutionary time,
so did the distance between the heart and the brain. To
pump blood 2 m to the brain of the extant giraffe requires
a larger heart and the highest known blood pressure in any
animal (Warren, 1974; Mitchell et al., 2006). Under the
sexual selection hypothesis, costs are expected to accompany sexually selected traits because they are conditiondependent (Andersson, 1994). While traits such as long tails
or long necks may attract predators (e.g. Petrie, 1992), the
individual doing so benefits from increased mating access.
Available evidence on predation is scanty for giraffe, but
males in a wild South African population suffered 1.8-fold
higher predation levels than females (Pienaar 1969), and the
108 giraffe killed (2% of the population) over 2 years
indicated that giraffe were the third most preferred prey for
lions Panthera leo. If giraffe live to an average of 25–28 years
(Dagg & Foster, 1976), their annual adult mortality (1/
longevity) should be less than 4% suggesting that lion
predation adds greatly to mortality. This may arise from the
behaviour of males persistently following oestrous females
or from physiological costs. Adult males have longer (Dagg
& Foster 1976) and proportionately larger necks than
females (this study), and have larger skeletons that require
more protein and calcium-rich browse (Mitchell & Skinner,
1993). Thus, males may lose condition quickly if food
becomes limiting, and this may lead to increased mortality.
It is critical, however, to determine the neck size of those
males suffering the highest predation, and whether males in
good condition grow the largest necks.
Phylogenetic evidence
The earliest obvious fossil ancestor of the giraffe Giraffokeryx punjabiensis had skeletally short legs and neck (Colbert,
1933; Badlangana et al., 2009), and occurred in India some
12–15 Mya (Mitchell & Skinner, 2003). The giraffid Paleotragus primaevus, similar in size to the okapi Okapia johnstoni, showed long legs but an unelongated neck and arose
about 12–15 Mya (Mitchell & Skinner, 2003) and went
extinct about 9 Mya. Among subsequent ancestors, the
medium-sized Paleotragus germaini and the large Samotherium sp. exhibited elongated necks relative to their total
vertebral column (Badlangana et al., 2009). Paleotragus
germaini was apparently the first species to show elongation
of modern giraffe proportions as reconstructed from fossil
cervical vertebrae (Badlangana et al., 2009). Samotherium
species that followed were also long necked but much larger
and dominated from about 9–5 Mya. Thus, giraffid necks
elongated during a period when the climate was cooling,
grasslands were expanding and rainfall was declining
(Mitchell & Skinner, 2003).
Under the competing browser hypothesis, legs should
have elongated at the same pace as necks (selection was on
reaching higher levels), whereas the sexual selection hypothesis predicts that neck length increased disproportionately
(as a runaway process). At present, the fossil record is too
patchy to support one hypothesis over the other. However,
the closely related okapi has a leg : neck ratio of c. 1:0.44
(Simmons & Scheepers, 1996) compared with the giraffe’s
1:1.13 (female) and 1:1.08 (male) (Mitchell et al., 2009). In
other words, necks have grown more than twofold longer in
c 2010 The Authors. Journal compilation c 2010 The Zoological Society of London
Journal of Zoology 282 (2010) 6–12 9
Giraffid evolution revisited
R. E. Simmons and R. Altwegg
giraffe relative to okapi. Given that okapi are similar in
proportion to the ancestral G. punjabiensis, (Colbert, 1938;
Savage & Long, 1986), ancestral giraffe have shown a
disproportionate lengthening of the neck and palaeontology
needs to inform us what precipitated and accompanied the
change from 1:0.44. Badlangana et al. (2009) determined the
increased length of the seven cervical vertebrae relative to
the overall vertebral column length. The neck vertebrae of
the okapi comprise 35% of the total vertebral column, while
that of the giraffe comprise 54%. Ancestral Paleotragus
species or Samotherium could not be resolved in the same
manner, but graphing the relative change in neck to the total
vertebral column would indicate when, and how fast, the
elongation occurred in the giraffe’s closest ancestors.
Long necks as a pre-requisite
for necking?
Some authors argue that ‘necking’ cannot have been the
origin of elongation because a long neck is required at the
incipient stages (Mitchell et al., 2009). The evolution of a
morphological trait comprises two parts: (1) the incipient
growth (origin) of the trait and (2) its present-day maintenance. Clarification of the incipient origin is often only
possible with a precise fossil record, showing forms before
and after the presumed event. Present-day maintenance is
easier to evaluate because intra-sexual competition, female
mate choice, predators and competition for resources can be
measured directly and the selective pressures quantified.
This point was clarified in Simmons & Scheepers, (1996)
when they stated that long necks may be an exaptation
(Gould & Vrba, 1982) – a trait arising from other selection
pressures and now ‘hijacked’ for other purposes. So the
tipping point does not have to be the same as the selection
pressures that either drove the neck ever longer or maintain
it present day. More arid climates and advancing grasslands
during the mid-to late Miocene (Mitchell & Skinner, 2003;
Badlangana et al., 2009) appear to have coincided with this
change. Simultaneously, the ancestral Palaeotraginae
moved into Africa where new habitats such as open treed
savannas existed (Mitchell & Skinner, 2003). These slightly
elongate animals may have adapted to their new environment by growing taller to feed off tall trees. Equally
plausible is an isometric change in body proportions with
an increasing body size (e.g. due to a cooler climate) that
increased the neck length beyond a point that disallowed
head-butting or wrestling. This would signal the beginning
of runaway sexually selected lengthening as one of the
prototype giraffids (e.g. Giraffokeryx or Paleotragus primaevus) switched exclusively to head clubbing.
Furthermore, the horns and ossicones used for combat in
several early ancestors were neither forward-facing (implying head-butting) nor antlered (implying head wrestling:
Caro et al. 2003), but were positioned laterally on the skull
to point almost perpendicular from it. This occurred in the
earliest known ancestor Canthumeryx sirtensis (Churcher,
1976) and was repeated by the four-horned Giraffokeryx,
with rather laterally orientated and backward-pointing
10
ossicones (Colbert, 1933). Neither exhibited elongated necks
of the proportion seen in giraffe. This positioning implies
that both species fought with sideway movements of the
head, possibly while standing side by side. This is precisely
the precursor one would predict for the longer swinging arcs
evident in the extant giraffe but without their elongated
necks. Further support comes from unpublished data suggesting that okapi males also exhibit side-to-side head
swinging as well as typical head butting (S. Shurter, pers.
comm.), implying that this is a deep-seated behavioural trait
common to giraffids.
Future tests – ossicones and necks
evolving in unison
We propose that the two main hypotheses can be distinguished by assessing the phylogenetic development of short
stout ossicones in conjunction with neck elongation. Traditionally, head wrestling is undertaken by ungulates with
antlers (e.g. Cervidae) or twisted and ribbed horns (e.g.
Antilopinae) that lock on contact, while head butting is
practised by species with massive curved horns (e.g. Caprinae) or frontal bosses (e.g. Bovinae) (Geist 1966, CluttonBrock, 1982; Estes, 1991; Caro et al., 2003). By contrast,
stout ossicones are used by male giraffe to concentrate the
force of a swinging head to sometimes splinter bones of
opposing males (Innis, 1958; Simmons & Scheepers, 1996).
Thus, if the origin of neck elongation occurred because of
competition over females rather than browse, the incipient
neck elongation should be accompanied by a change in horn
morphology from large antlers to small, stout ossicones.
The giraffid fossil record should indicate at what stage the
small sideways pointing horns of the ancestral giraffids (e.g.
Canthumeryx sirtensis Churcher, 1976) evolved to the short
blunt ossicones we see on the extinct long-necked Samotherium and all subsequent giraffids (Colbert, 1933; Mitchell &
Skinner 2003; Badlangana et al., 2009). Simultaneously, we
should see a change in the relative length of the neck and
forelegs. The sexual selection hypothesis predicts that the
appearance of ossicones is most likely to coincide with the
time that the neck becomes slightly too long for wrestling or
butting, and this in turn should lie at the start of an
allometric departure from isometric neck length to foreleg
length ratios. Neck elongation should also coincide with
sexual dimorphism in the skulls of ancestral giraffids.
Natural selection predicts that the neck and leg elongation
should co-occur, but it makes no predictions concerning
skull dimorphism.
Main challenges for both
hypotheses remain
Our review of evolutionary hypotheses explaining the giraffe’s long neck shows that both main hypotheses have
merits and challenges. For the competing browsers hypothesis, we need to determine what maintains modern giraffe
c. 2.5 m above possible competitors when there are costs in
terms of predation rate, blood pressure and maintenance of
c 2010 The Authors. Journal compilation c 2010 The Zoological Society of London
Journal of Zoology 282 (2010) 6–12 R. E. Simmons and R. Altwegg
skeletal lengthening (Warren, 1974; Mitchell et al., 2006).
An animal approximately half the size of the present-day
giraffe (i.e.2.5–3.0 m high) would be sufficient to outcompete other folivores. The main challenge for the sexual
selection hypothesis is to explain why female giraffes also
have long necks, even though their necks are shorter than
those of males. Genetic correlation between the sexes is one
reason for male-like characters (Darwin, 1871, Fisher, 1930,
Lande 1987, but see Stankowich & Caro, 2009), and the
small ossicones of female giraffe are more likely to arise
from such correlations than female–female competition. If,
however, there are costs to having a long neck and no
benefits to females, genetic correlations between female and
male neck length may break down and result in more
pronounced dimorphism. Estimates of the genetic correlation between female and male neck characteristics are
required together with precise estimates of the physiological
costs to determine whether the long female neck is a byproduct of selection on males. The competing browser
hypothesis proposes benefits for both sexes, and a reduction
in competition between the sexes through foraging height
partitioning is a possible advantage that remains unexplored. In the absence of direct selection on neck length
under sexual selection, it may be sufficient to propose that
the shorter necks of females (and the lack of growth after
8 years: Simmons & Scheepers, 1996) is one way of reducing
physiological and heart-to-head costs.
We conclude that both mechanisms may play a role in the
origin and maintenance of this unique trait and suggest that
refined measurements of costs and selection pressure together with a fresh look at the fossil record should allow us
to quantify their relative importance.
Acknowledgements
Numerous discussants have helped shape our ideas and we
especially thank Phoebe Barnard, Elissa Cameron, David
Cumming, Raoul du Toit, Julian Fennessy, Terese Hart,
Paul Manger, Anders Møller, Steve Shurter, Colleen Seymour and Russ Seymour for their thoughts or data. Reviews
by Johan du Toit and three anonymous referees assisted our
presentation.
References
Andersson, M. (1994). Sexual selection. New Jersey: Princeton University Press.
Badlangana, N.L., Adams, J.W. & Manger, P.R. (2009). The
giraffe (Giraffa camelopardalis) cervical vertebral column: a
heuristic example in understanding evolutionary process?
Zool. J. Linnean Soc. 155, 736–757.
Bergeron, P., Festa-Bianchet, M., von Hardenberg, A. &
Bassano, B. (2008). Heterogeneity in male horn growth and
longevity in a highly sexually dimorphic ungulate. Oikos
117, 77–82.
Giraffid evolution revisited
Bonduriansky, R. (2007). Sexual selection and allometry: a
critical reappraisal of the evidence and ideas. Evolution 61,
838–849.
Brand, R. (2007) Evolutionary ecology of giraffes (Giraffa
camelopardalis) in Etosha National Park, Namibia. PhD
thesis, Newcastle University, UK.
Cameron, E.Z. & du Toit, J.T. (2007). Winning by a neck: tall
giraffes avoid competing with shorter browsers. Am. Nat.
169, 130–135.
Caro, T.M., Graham, C.M., Stoner, C.J. & Flores, M.M.
(2003). Correlates of horn and antler shape in bovids and
cervids. Behav. Ecol. Sociobiol. 55, 32–41.
Churcher, C.S. (1976). Giraffidae. In Evolution of mammals in
Africa: 509–535. Maglio, V.J. (Ed.). Princeton: Princeton
University Press.
Clutton-Brock, T.H. (1982). The function of antlers. Behaviour 79, 108–121.
Clutton-Brock, T.H., Albon, S.D. & Harvey, P. (1980).
Antlers, body size and breeding group size in the Cervidae.
Nature 285, 565–567.
Colbert, E.H. (1933). A skull and mandible of Giraffokeryx
punjabiensis (Pilgrim). Am. Mus. Novitates 632, 1–14.
Colbert, E.H. (1938). The relationships of the Okapi.
J Mammal. 19, 47–64.
Cuervo, J.J. & Moller, AP. (2009). The allometric pattern of
sexually size dimorphic feather ornaments and factors
affecting allometry. J. Evol. Biol. in press, doi: 10.1111/
j.1420-9101.2009.01758.x
Dagg, A.I. & Foster, J.B. (1976). The giraffe, its biology,
behaviour and ecology. New York: Van Nostrand Reinhold.
Darwin, C. (1871). The descent of man and selection in relation
to sex. London: John Murray.
Du Toit, J.T. (1990). Feeding height stratification among
African browsing ruminants. Afr. J Ecol. 28, 55–61.
Du Toit, J.T. (1995). Sexual segregation in kudu: sex differences in competitive ability, predation risk or nutritional
needs? S. Afr. J. Wildl. Res. 25, 127–132.
Estes, R.D. (1991). The behaviour guide to African mammals.
Chicago: University of Chicago Press.
Fisher, R.A. (1930). The genetical theory of natural selection.
Oxford: Clarendon Press.
Geist, V. (1966). The evolution of horn-like organs. Behaviour
27, 175–214.
Ginnett, T.F. & Demment, M.W. (1997). Sex differences in
giraffe foraging behaviour at two spatial scales. Oecologia
110, 291–300.
Gould, S.J. & Vrba, E. (1982). Exaptation – a missing term in
the science of form. Paleobiology 8, 4–15.
Innis, A.C. (1958). The behaviour of the giraffe Giraffa
camelopardalis in the eastern Transvaal. Proc. Zool. Soc.
Lond. 131, 245–278.
Kodric-Brown, A. & Brown, J.H. (1984). Truth in advertising: the kinds of traits favoured by sexual selection. Am.
Nat. 124, 309–323.
c 2010 The Authors. Journal compilation c 2010 The Zoological Society of London
Journal of Zoology 282 (2010) 6–12 11
Giraffid evolution revisited
R. E. Simmons and R. Altwegg
Kodric-Brown, A., Sibly, R.M. & Brown, J.H. (2006). The
allometry of ornaments and weapons. Proc. Natl. Acad.
Sci. USA 103, 8733–8738.
Lande, R. (1987). Genetic correlations between sexes in the
evolution of sexual dimorphism and mating preferences. In
Sexual selection: testing the alternatives. Bradbury, J.W. &
Anderson, M.B. (Eds). Chichester: Wiley.
Malo, A.F., Roldan, E.R.S., Garde, J., Soler, A.J &
Gomendio, M. (2005). Antlers honestly advertise sperm
production and quality. Proc. Roy. Soc. Lond. B. 272,
149–157.
Mitchell, G., Maloney, S.K., Mitchell, D. & Keegan, D.J.
(2006). The origin of mean arterial and jugular venous
blood pressures in giraffes. J. Expt. Biol. 209, 2515–2524.
Mitchell, G., van Sittert, S.J. & Skinner, J.D. (2009). Sexual
selection is not the origin of the long neck of the giraffe.
J. Zool. (Lond.) 278, 259–269.
Mitchell, G. & Skinner, J.D. (1993). How giraffe Giraffe
camelopardalis adapt to their extraordinary shape. Trans.
Roy. Soc. S. Afr. 48, 207–218.
Mitchell, G. & Skinner, J.D. (2003). On the origin, evolution
and phylogeny of giraffe Giraffa camelopardalis. Trans.
Roy. Soc. S. Afr. 58, 51–73.
Petrie, M. (1992). Peacocks with low mating success are more
likely to suffer predation. Anim. Behav. 44, e585–e586.
Pienaar, U. & de V. (1969). Predator-prey relationships in the
Kruger National Park. Koedoe 12, 108–176.
Pratt, D.M. & Anderson, V.H. (1982). Population, distribution, and behaviour of giraffe in the Arusha National Park,
Tanzania. J Nat. Hist. 16, 481–489.
Pratt, D.M. & Anderson, V.H. (1985). Giraffe social behaviour. J. Nat. Hist. 19, 771–781.
R Development Core Team. (2009). R: A language and
environment for statistical computing, 2.9.0. ISBN
3-900051-07-0. Vienna: R Foundation for Statistical Computing: Available at http://www.R-project.org.
Roulin, A.R., Altwegg, H., Jensen, I., Steinsland, & Schaub,
M. (2010). Sex-dependent selection on an autosomal
12
melanic female ornament promotes the evolution of sex
ratio bias. Ecol. Lett. 13, 616–626.
Savage, R.J.G. & Long, M.R. (1986). Mammal evolution: an
illustrated guide. London: British Museum (Natural History).
Senter, P. (2007). Necks for sex: sexual selection as an
explanation for long necks in sauropod dinosaur neck
elongation. J. Zool. (Lond.) 271, 45–53.
Seymour, R. (2001) Patterns of Subspecies Diversity in the
Giraffe, Giraffa camelopardalis (L. 1758): Comparison of
Systematic Methods and their Implications for Conservation
Policy. PhD thesis
Shorrocks, B. (2009). The behaviour of reticulated giraffe in
the Laikipia district of Kenya. Giraffa 3, 22–24.
Simmons, R.E. (2008). Tall tales: or how the giraffe got its
neck. Afr. Geogr. 16, 32–39.
Simmons, R.E. & Scheepers, L. (1996). Winning by a neck:
sexual selection in the evolution of giraffe. Am. Nat. 148,
771–786.
Smithers, R.H.N. (1983). The mammals of the southern
African subregion. Pretoria, South Africa: University of
Pretoria: pp 562–566.
Stankowich, T. & Caro, T. 2009. Evolution of female weaponry in female bovids. Proc. Roy. Soc. Lond. Ser. B 276,
4329–4334.
Vanpe, C., Gaillard, J.-M., Kjellander, P., Mysterud, A.,
Magnien, P., Delorme, D., Van Laere, G., Klein, F.,
Liberg, O. & Hewison, A.J.M. (2007). Antler size provides
an honest signal of male phenotypic quality in Roe Deer.
Am. Nat. 169, 481–493.
Warren, J.V. (1974). The physiology of the giraffe. Sci. Am.
231, 96–105.
Woolnough, A.P. & du Toit, J.T. (2001). Vertical zonation of
browse quality in tree canopies exposed to a size-structured
guild of Africa browsing ungulates. Oecologia 129,
585–590.
Young, T.P. & Isbell, L.A. (1991). Sex differences in giraffe
feeding ecology: energetics and social constraints. Ethology
87, 79–89.
c 2010 The Authors. Journal compilation c 2010 The Zoological Society of London
Journal of Zoology 282 (2010) 6–12