One Basket or Many?
Our society is obsessed with sex. Small wonder: sex humbles by reminding us of our animal origins and ultimate mortality, bringing to the human experience some of our most sublime — and most ridiculous — moments. Now, I'm as enthusiastic about sex as the next person, but there's more to my abiding interest than what Saturday Night Live's ultra-pious Church Lady used to call "tingly naughty bits".
As a biologist, I am interested in how and why organisms do what they do. Studies indicate that all living creatures are (in their own way) 'obsessed' with sex. Two of the most powerful drives motivating any living creature are feeding and reproduction. And a pretty good case could be made that the main reason any animal eats is so it has the strength to schtup. The urge to mate is powerful, indeed. Everyone who understands what 'puberty' means is aware that much pleasure is derived from the release of sexual tension. And observations of other creatures suggest that many of them enjoy sex as much as humans do.
Intellectually, most of us know that sex is fun in order to ensure continuance of a bloodline. But why is that important? It's all part of a four billion-year-old game of chance I call the 'Darwinian Lottery'. Here's how the game works: a parent stakes its young against an uncertain environment; the parent 'wins' if its young survive to play another round. Put another way, the Darwinian Lottery is a parent's way of having at least some of its genes represented in future generations. It's not as good as being there personally, but being represented by proxy is better than not being represented at all. Thus, the stakes in the Darwinian Lottery are nothing less than a kind of genetic immortality. In order to achieve the sort of mutual understanding and co-operation necessary for successful mating, a remarkable range of reproductive organs and behaviors has evolved. The processes of natural selection have sculpted and refined these gene-transfer technologies, and sexually reproducing organisms have been having a lot of fun ever since.
But, as in any game of chance, there are many reproductive strategies a parent might adopt in playing the Darwinian Lottery. In the race for genetic immortality, is it evolutionarily more successful to put all your eggs in one basket or many? The relatively new field of theoretical ecology provides some illuminating answers and surprising implications. Despite its youth, theoretical ecology is already heavy and opaque with jargon, abstract concepts, and mathematics. To fully explore how these erudite matters apply to reproductive strategy would strain my teaching ability and probably your patience as well. Fortunately, some aspects of theoretical ecology can be appreciated without having to tackle much jargon or any mathematics (Whew!).
Like whales and humans, sharks are K-selected animals, meaning they adhere to a life history strategy featuring slow growth, delayed maturation, long gestation, and the production of few, precocial young. These are Silvertip Sharks (Carcharhinus albimarginatus), which grow only centimetres per year, reach maturity at perhaps 7 or 8 years of age, and typically have only 5 to 6 pups after a gestation period of about a year.
Photo © David Fleetham david@davidfleetham.com; used with the gracious permission of the photographer.
About 40 years ago, ecologist Robert McArthur developed an elegant system for describing the stability and age distribution of natural populations known as 'r/K selection'. Now, 'r' and 'K' are symbols in numerous equations of theoretical ecology, representing components of an organism's life history strategy (reproductive capacity and environmental carrying capacity, respectively). But 'r' and 'K' are intimately associated with diametrically opposed reproductive strategies. Since 'r' selected organisms tend to invest their reproductive effort in massive, all-or-nothing spawnings, I prefer to call them 'Big Bang' strategists. Big Bang strategists tend to spew bazillions of tiny, poorly-formed young into the environment, providing little or no parental care afterward. Conversely, 'K' selected organisms invest their reproductive effort toward the production of few, large, well-developed young and protect their genetic investment through prolonged parental care — so I prefer to call them 'Many Basket' strategists. In terms of winning the Darwinian Lottery, which of these strategies is 'better'?
It is important to bear in mind that no organism is completely 'r' or 'K' selected. Big Bang and Many Basket are merely convenient theoretical models, representing opposite poles on a continuous spectrum of reproductive strategies. But a look at the life histories of two creatures rather far apart on this continuum may best illustrate the relative virtues and short-comings of each of these strategies. In this corner, representing the Big Bang strategy, is the Opalescent or Market Squid (Lologo opalescens ); and in the opposite corner, representing the Many Basket strategy, is the Sperm Whale (Physeter macrocephalus ). I have deliberately chosen two creatures that can be observed by divers or mariners, form a natural predator-prey system, and have been harvested commercially.
Every winter — especially during nights with a 'new' moon — millions of Opalescent Squid aggregate in shallow waters along the Pacific coast to breed. These mature squid — each about 20 cm long and a year old — move inshore and begin courtship and mating. Males woo ripe females with a dazzling Technicolor display, their chromatophores (specialized color cells) expanding and contracting to send waves of iridescent red, yellow, brown, and gold along their bodies. When the female blanches, this signals the male to seize her head-on and begin copulation. The fourth left arm of each mature male is specialized with hundreds of tiny suckers; this arm, called a 'hectocotylus' (from the Latin, meaning "I don't know where to start counting, either!") is used to transfer a spermatophore (sperm packet containing tens of thousands of gametes) into the mantle cavity of the female. This coupling lasts perhaps ten seconds. During mating and copulation, the squids are quite unresponsive to danger, and predators — particularly commercial fishermen and Blue Sharks — congregate to take advantage of this impassioned calamari. Only by synchronizing their spawnings in massive reproductive orgies can Opalescent Squid stand a chance to glut the predator market so a few of their young may survive to continue playing the Darwinian Lottery.
After fertilization, the female deposits her eggs in 20 to 30 translucent white sausage-shaped egg cases, each about as long as the mother squid and containing 180 to 300 eggs. The egg cases are attached to the bottom in sheltered locations, usually on flat areas of mud or sand at an average depth of about 40 metres. Most squids die shortly after spawning, and thus parental care is impossible. The egg cases are vulnerable to predators, including bottom-dwelling elasmobranchs such as Angel and Horn Sharks. But since clusters of egg cases ('sea mops') may cover some 90 hectares of sea bottom and are all deposited at about the same time, usually a few escape predation. Development of the embryos may last from three weeks up to three months, depending upon water temperature. After hatching, the infant squid live for the first few days on nourishment from the yolk sac. Early prey of these 'squidlets' appear to be tiny planktonic crustaceans. The young squid grow rapidly, remaining in the surface plankton until they reach a mantle length of about 4 cm — at which time they move closer to the bottom. When the squid young reach a mantle length of about 8 cm, they begin to school with older individuals and feed on fishes, crustaceans, and smaller squids. The young that survive return in a year to begin the cycle anew.
The total lifespan of the Opalescent Squid is estimated to be less than two years. Thus these Big Bang strategists probably have only one chance to perpetuate their genes. One of the characteristics of Big Bang strategists is that their populations are subject to wide fluctuations of relative abundance. If environmental conditions happen to be optimal, a Big Bang strategist's potential representation in future generations may be enormous. If environmental conditions happen to be suboptimal or poor, very few or none of a Big Bang strategist's young may survive to breed. This 'hit or miss' quality of Big Bang strategists makes them excellent colonizers of new or unstable environments and is responsible for the phenomenon known as 'year class' among commercial fisheries — some years, you're up to your armpits in squid (or whatever), others you have to take out another mortgage on the boat because you couldn't catch enough to make the bank payments. But most of the time, Big Bang strategy seems to work out for the Opalescent Squid. Good thing, too — as most frozen squid found in North American fish markets and food stores are of this species. Opalescent Squid are taken by net in huge numbers — more than five tonnes per hour — during the nights they enter shallow water to breed.
Near the other end of the reproductive — and size — spectrum is the great Sperm Whale. Immortalized in Herman Melville's Moby Dick, for most people the Sperm Whale has come to epitomize the essence of 'whale-ness'. But the Sperm Whale remains a creature more of art and commerce than of science. With its massive, rectangular and lop-sided head and 'wrinkled' flanks, the Sperm Whale is one of the most bizarre animals on earth. Sperm Whales are also by far the largest predatory animal on our planet. Males grow to a length of 15 to 18 metres and a mass of up to 55 tonnes; females may attain 10 to 12 metres in length and up to 16 tonnes in mass. Although sometimes encountered near oceanic islands, Sperm Whales typically inhabit open ocean seaward of continental shelves; only recently have details of their life history begun coming to light. Although fishes and other items are occasionally consumed, the search for squid accounts for much of the behavior and biology of the Sperm Whale. Each day a large male Sperm Whale may eat about 3.5% of its body weight in squid. Many other cetaceans hunt squid, often in the same locations as do Sperm Whales, but the evolution of extraordinary adaptations has allowed this species to escape competition by feeding at depths far beyond those attainable by any other mammal.
The social structure of Sperm Whale populations is complex. Females, including those which are pregnant or nursing, calves and some juveniles swim in 'mixed' or 'nursery pods' averaging about 25 individuals. When males reach puberty at about age 9, they may join 'bachelor pods' of up to 10 whales. During the breeding season in spring and early summer, large males compete for control of sexually mature females, which are usually over 8.5 metres in length, 6.3 tonnes in mass, and 8 years old. Battles over females probably occur, judging from Sperm Whale tooth marks that scar the skin of most males. Successful males obtain exclusive breeding rights to 'harems' averaging 10 females. Although males attain sexual maturity at 11.9 metres, 18 tonnes, and 19 years of age, a male probably has no opportunity to mate until he achieves 'social maturity' by deposing a reigning harem-master bull in battle. Harem masters are usually 13.7 metres long, 27 tonnes, and 25 years of age. Large old bulls without harems swim singly or in small groups throughout the year, venturing during summer into cold water of high latitudes. Females and young Sperm Whales generally remain within the Atlantic, Pacific, and Indian Ocean areas bounded by 45° south to 45° north latitude.
The reproductive rate of the Sperm Whale is one of the slowest among whales. Gestation lasts about 15 months and the 4-metre, 998-kilogram calf nurses for two years, during which time it will grow to 6.7 metres and about 2.7 tonnes. A female probably does not become pregnant for another 9 months after weaning ends; thus, the rate of calving is about once every 4 years. By investing so much parental effort in their young, Sperm Whales maximize the chances that each individual calf will grow to maturity, making them classic Many Basket strategists. This strategy is highly successful in relatively stable environments, but makes Many Basket strategists vulnerable to overharvesting. The Sperm Whale had been the mainstay of the great American whaling fleet during the 18th and 19th centuries. Awareness of the slow reproductive rate and uncertainty about the effects on reproduction of changes in sex ratios and population structures caused by hunting led the International Whaling Commission (IWC) to pass a zero quota resolution, under which no Sperm Whales were to be caught anywhere for three years starting in 1981. A number of non-IWC nations continued to harvest Sperm Whales, and some stocks now show serious indications of decline. The current world population of Sperm Whales is more than 500,000 strong. With the pressure of public opinion mounting against whaling and whale products, there is currently every indication that Sperm Whales will outlast the industry which has for so long hunted them.
Thus, different reproductive strategies tend to be successful in different environments — Big Bang in new or unstable habitats, Many Basket in established, stable ones. A major shortcoming of asexual reproduction is that, all things going well, each and every 'daughter' is genetically identical to its parent. Any environmental change that would kill a parent would more than likely kill all its progeny as well. Game-Over: big-time loss in the Darwinian Lottery. Before microbes 'invented' sex some 2.2 billion years ago, the main sources of new genetic combinations were mutation and transcription (gene duplication) errors. Evolution must have occurred at a glacial pace. With the development of sex, progeny were genetically different from either parent and the rate of evolution was greatly accelerated. With different combinations of genes coding for different phenotypic (physical) abilities and limitations, the odds that at least some of a parent's young would have the 'right stuff' to survive to breed were vastly improved; so was a parent's likelihood of genetic representation in future generations. By shuffling gene combinations and adding to them, sex has enabled the diversity of life to flower into the riot of forms and lifestyles we see today.
The common currency of inheritance — the nucleic acids DNA and RNA — is too extraordinarily complex and 'clunky' to have evolved independently more than once. For all its incredible diversity, all life is interrelated to some degree. In our very own personal bodies, you and I carry some of the genetic hand-me-downs of the very earliest lifeforms — a rather humbling thought. That each of us is intimately interconnected with all earthly life by a web of genetic heritage that embraces 10 million species and spans nearly four billion years is an awesome, spine-tingling, and altogether mind-blowing idea. Some creatures — especially Many Basket strategists — complete their life cycles on a timescale much longer than our ability to harvest or eradicate them. Each time a species becomes extinct through human carelessness, we lose an irreplaceable part of our natural heritage.
Regular readers of my work have doubtless noticed that I always try to squeeze my subject matter into a larger context. While most of the time these 'larger contexts' are pretty much academic (usually ecology or evolution), herein lies a nugget of genuinely practical use: the deeply biological reason why men and women will probably never see eye to eye on the subject of sex.
You see, sperm is relatively inexpensive to produce in quantity (being little more than a nucleus of DNA with a delivery system). So, if you're male, the factor which most limits your potential representation in future generations is mate acquisition — and your best strategy for winning the Darwinian Lottery is, to put it bluntly, disseminate and inseminate as widely as possible. Ova are rather more expensive to produce (including not only genetic material, but also yolk and certain cellular constituents — such as mitochondria). Since females can almost always find a randy male who is more than willing to share a bit of his genetic material, the chief factor limiting a female's reproductive success is resource acquisition — including sufficient energy stores to produce worthwhile clutches of eggs and perhaps a male who will stick around to help her raise their young.
Thus, the sexes have fundamentally opposite strategies for winning the Darwinian Lottery: males are primarily concerned with mate acquisition and females with resource acquisition — which is why men tend to be polygamous and women monogamous. What I want to know is: why in our society has female 'resource acquisition' become synonymous with 'shoes'? ;-)
An abridged version of this was originally published in Diver Magazine December 1993
