A leg up, and a neck up, on the competition



Giraffe (Giraffa camelopardalis) at the the Cincinnati ZooOK, let’s face it giraffes (Giraffa camelopardalis) are just plain cool. Tall and lanky Manute Bols of the animal world covered in spots. In addition to being high on the list of must-see animals on an African safari, giraffes have served as poster children for evolution. Long before Darwin, that other evolutionist, the French naturalist Jean-Baptiste Lamarck, speculated that the long-necked giraffe was descended from shorter-necked ancestors. According to Lamarck, all that stretching to get to juicy, tree-top leaves changed their necks in ways that they then passed on to their offspring.

The giraffe lives in dry, desert places, without herbage, so that it is obliged to browse on the leaves of trees, and is continually forced to reach up to them. It results from this habit, continued for a long time in all the individuals of its species, that its fore limbs have become so elongated that the giraffe, without raising itself erect on its hind legs, raises its head and reaches six meters high (almost twenty feet).” Lamarck on giraffes taken from Alpheus Spring Packard. 1901. Lamarck, the founder of evolution: his life and work with translations of his writings on organic evolution. Longmans, Green and Co.

Along comes Darwin who bought into the idea that living things can change over time but didn’t buy into Lamarck’s mechanism for evolution. For Darwin the evolution of the giraffe’s elongated neck was due to selection. From the standpoint of Darwin’s natural selection individuals in ancestral giraffe populations varied in some intrinsic and immutable way, at least immutable in the lifetime of an individual. These ancestral giraffes not only varied in leg and neck length but they also varied in their propensity to survive and contribute offspring to the population. Variation in survival and reproduction was in turn correlated to some variation in physical traits. Proto-giraffes that survived and successfully bred (one usually is necessary for the other) then passed on their intrinsic “legginess” and “neckiness” to their progeny and the population changed over time, generation-by-generation getting a little taller and necks a little longer as selection sieved through that variation in the population that can be passed from parent to offspring. It’s remarkable that Darwin came up with natural selection while knowing next to nothing about exactly how traits were passed from parent to offspring. It wasn’t until nearly a century after Darwin that natural selection was reconciled with the viable model of biological inheritance we call genetics.

But where are we then left with giraffes? Clearly neck and leg length evolved and likely by some sort of Darwinian selection in giraffes. Giraffes’ closest living relatives, the equally cool, West-African forest dwellers, the Okapi (Okapia johnstoni), have comparatively short necks and the fossil record reveals many giraffes with short necks. Modern giraffes are nested in a family tree that therefore points to short-necked ancestors. But, if selection plays a role then what is the agent of that selection? Darwin posed two models of selection; good-ole-fashioned natural selection where predators, the physical environment, competition for food, parasites or some other agent act on survival and reproduction and sexual selection where the agent of selection lies in a species’ own gene pool. In sexual selection the variance in individuals contribution to the population stems from competition for mates, either competition with members of your own sex to access the opposite sex or competition imposed by a choosy opposite sex. These forms of selection, natural and sexual, are basically the same, both involve filtering through available variation to change the population, but in sexual selection the agent of selection lies specifically in competition for mates. Competition for mates can lead some some crazy characteristics, everything from a moose’s antlers to the gaudy flowers of orchids, and maybe giraffes necks?

In a new paper in the Journal of Zoology researchers at the University of Cape Town and the South African National Biodiversity Institute review the evidence for the relative  contributions of natural and sexual selection to the evolution of the giraffe’s neck. Two hypotheses have attempted to explain long necks in giraffes. One invokes natural selection and says that competition with other browsers in Sub-Saharan Africa generates selection favoring those members of the population who can reach a little higher into the trees. The other explains neck size in terms of the dramatic contests that males have over access to females. Male giraffes in the breeding season line up side-to-side, brace themselves by spreading their front legs out and proceed to pommel one another with those massive necks. The force of the blow can shatter the ribs of an opponent and deaths in these contests are not unheard of. Additionally the females are apparently not passive trophies to be won as the result of some pounding between males but they may exercise some mate choice based at least partially on a long, handsome neck.

Here’s the rub. Contrary to what one would expect based on the natural selection scenario, giraffes are a good 2 meters taller than their closest competitors and, despite Lamarck’s musings on their feeding habits, in many giraffe populations individuals often feed at shoulder height rather than reaching for the tippy-top of the trees. Also, if the primary benefit to having a long neck, and long legs, was to reach higher to avoid competing with shorter rivals then both males and females should have similar sized necks, but they don’t. In populations studied in both Namibia and Zimbabwe, males are not only larger than females but have comparatively longer necks, and bigger heads, for their body size. While both males and females need to eat and browse leaves from trees, only males fight using that huge neck to club a rival to submission suggesting that the difference in size-corrected neck and head size in males is due to selection imposed on males from fighting. Also, giraffe necks are elongated due to virtue of longer vertebrae not necessarily more vertebrate and when compared to the Okapi and fossil giraffes the size of the neck bones in living giraffes is larger relative to the vertebrae in the rest of their body. During contests the combatant with the larger neck tends to come out on the winning side of the battle, although the relative contribution of large necked males to the next generation is not known. The absence of paternity data notwithstanding, there seems to be something about the neck per se rather than just overall height suggesting a role for sexual selection.

The authors state that a prediction of the natural selection or “competing browser’ hypothesis is that it is height, not necessarily neck length, that is under selection. This means that leg length and neck length should be under similar selective pressure and should evolve at the same rate. They don’t. When comparing modern giraffes, Okapi and their fossil relatives the authors report a rate of evolution for necks twice that of legs in the modern giraffe lineage. Of course a potential defense of the “competing browser’ idea is that it may be that it is easier for giraffe populations to respond to selection to be the tallest browsers on the savannah by growing their necks than their legs. Trade-offs in growth and development and limitations in the available genetic variation in the population can shift the population’s response to selection away from one where evolution of legs and necks occurs at equal rates.

All of the evidence is pointing towards an important role for sexual selection in the evolution of the giraffe neck, but, why do females have long necks? The authors cite this a major challenge for the sexual selection hypothesis, but, really it is easily explained by the fact that, unlike some structure unique to a male, both males and females have necks and heads and the genes to make necks and heads. Long necked males successful in the fighting arena not only pass on genes for long necks to their male offspring but to female offspring as well. Differential rate and timing of development between males and females, likely mediated by sex determining genes only on male Y-chromosomes then help contribute to the differences between males and females in size. The authors point out that more needs to be known about the heritability of neck length and the costs to females for having comparatively longer necks. Maybe the giraffe genome needs to be sequenced to start parsing out genes that influence growth and development? Sounds like a fun project to me.

Other unstudied aspects of giraffe neck evolution lie in the potential differences in foraging habits between males and females. Given that the dramatic differences in bill size and shape between male and female Purple-throated Caribs (Eulampis jugularis) are due to differences in flower preferences during foraging (Temeles et al. Science 2000) there is a precedent for this hypothesis in other animals. Also comparing different giraffe populations may be interesting. Selection may not be acting the same on all populations and the relative contributions of sexual selection and “competitive browsing” may differ substantially among populations. Brown et al. in a genetic study of giraffes published in the journal BMC Biology in 2000 found that different giraffe populations fall into at least 6 distinct genetic lineages and these lineages correspond with different spot patterns.

It is important to note that sexual and natural selection are not either-or rather both are a form of selection operating on the population, just in the case of sexual selection selection stemming specifically from competition for mating opportunities. Both sexual and natural selection operate simultaneously on an organism’s characteristics and often work in opposition to one another creating trade-offs between the best trait for competing for mates and the best trait for some other aspect of survival and reproduction.

So, what is cool about giraffes is not just their lanky good-looks but the fact that they have been telling us things about evolution ever since Lamarck.

Simmons, R., & Altwegg, R. (2010). Necks-for-sex or competing browsers? A critique of ideas on the evolution of giraffe Journal of Zoology, 282 (1), 6-12 DOI: 10.1111/j.1469-7998.2010.00711.x

Temeles, E. (2000). Evidence for Ecological Causation of Sexual Dimorphism in a Hummingbird Science, 289 (5478), 441-443 DOI: 10.1126/science.289.5478.441

Brown, D., Brenneman, R., Koepfli, K., Pollinger, J., Milá, B., Georgiadis, N., Louis, E., Grether, G., Jacobs, D., & Wayne, R. (2007). Extensive population genetic structure in the giraffe BMC Biology, 5 (1) DOI: 10.1186/1741-7007-5-57