A Buzz in the Meadow (29 page)

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Authors: Dave Goulson

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In bumblebees, inbreeding can lead to some rather peculiar gender-bending side-effects. To understand them requires a little diversion into how sex is determined in bumblebees. In many animals (including ourselves) sex is determined by which sex chromosomes we inherit. If we get an X and a Y, we are male; two Xs and we are female (some animals do it the other way round). In bees, it is quite different; sex is determined by a single gene. If an individual has two different copies of this gene, it is female. If it has two identical copies, or just one copy, it is male. Female bees, like us, have two copies of each chromosome – to use the technical term, they are diploid. In a genetically healthy population there are usually lots of different versions of the sex-determining gene, so the chances are that diploid individuals will have two different copies and thus will be female. Male bees, typically, have just one copy of each chromosome – they are haploid. To produce a son, a female bee has just to lay an unfertilised egg; the haploid gamete develops into a healthy son. This means that male bees have no father. To produce a daughter, the female bee fertilises her egg using sperm from a male; in bumblebees this sperm had been stored inside the queen since she mated the previous summer. So long as the copy of the sex-determining gene in the sperm is different from each of the two different copies held by the mother, then these diploid offspring will all be female.

The problem arises when the population is small. As I have said, small populations tend to lose genetic diversity through drift, so the number of versions of the sex-determining gene declines over time. Also, individuals soon become related to one another, so the chances that one of the queen's sex-determining genes and the male's match becomes more and more likely. If they do, then half of the queen's diploid offspring will have two identical sex-determining genes. This is a disaster for the nest, for these individuals develop as ‘diploid males', which do no work for the colony. Essentially half of the colony's workforce is useless – worse than useless, since they place a burden on resources, eating the food stores and not replacing them. This might not be so bad if the diploid males went out and mated with new queens, but diploid males seem to have lower fertility than normal males, and in any case the nest starts to produce them right at the beginning of the season, when there are no virgin queens around to mate with. With half their workforce sitting around idly scoffing food, we might expect such nests to die out long before other nests start to produce new queens in high summer.

Oddly enough, this is not how it seems to work out, and we don't yet know why. The presence of diploid males can be used as a warning sign of inbreeding in bees, and my PhD student Ben Darvill screened populations of some rare species, such as the moss carder bee, to see which populations are becoming inbred. He focused on the Hebrides, another island system where agriculture has changed relatively little and patches of flower-rich grassland are common. On the smaller, more remote islands of the Hebrides such as the Monach Isles, a tiny cluster of beautiful, sandy-shored islands off the west coast of North Uist, he found that diploid males were quite common. The unexpected thing was that some of the remaining bees were triploids – they had three sets of chromosomes.

Triploids look and act like female bees. They are presumably produced by diploid males successfully mating with a normal, diploid queen, against all the odds. This requires a nest producing diploid males to survive long enough to produce these males in late summer when new queens are on the wing, and then for the diploid males to outcompete normal, healthy haploid males in finding and courting a virgin female, and finally to produce viable (but diploid) sperm, despite their supposed low fertility. On the Monachs one in five of the female bees turned out to be triploids. Clearly diploid males are not quite as hopeless as was thought. Nonetheless, we now have other evidence that the inbreeding that leads to diploid male production also has other harmful side-effects. Small, isolated bumblebee populations have measurably lower genetic diversity than the larger populations, and rare species tend to have much lower genetic diversity than the common ones. What is more, Penelope Whitehorn has found that the more inbred populations suffer from higher loads of the internal parasite
Crithidia bombi
, presumably a sign of their generally low vigour. We do not yet have a data set to compare with Hanski's butterfly study, but I would hazard a guess that these small, isolated bumblebee populations, with little genetic diversity, high levels of diploid males and high parasite load, are probably not long for this world. However, if the population on the Monach Isles disappears it would not be a disaster as there are still plenty of bigger, less-isolated habitat patches on the larger Hebridean islands. The Monach Isles might well be recolonised in the future, and we would predict that the moss carder bee population there will continue to blink in and out of existence every few years, just as many of Hanski's butterfly populations do.

There are important lessons to be learned from all of this. The survival of the metapopulation as a whole depends upon colonisation events balancing extinctions. If the extinction of populations occurs faster than new ones are created, then the number of occupied patches will slowly decline over time, until eventually there are none. In the Åland islands, where the human population is low and agriculture is not intensive, there are still lots of habitat patches, and many of them are close together. Hence it is easy for unoccupied patches to be recolonised, and so new populations spring up as fast as old ones become extinct. Overall, Glanville fritillaries are doing just fine in the region. Similarly, moss carder bees are doing okay in the Hebrides. But imagine what would happen if a few of the habitat patches are destroyed. The average distance between patches of meadow will then be a little greater, slightly reducing the colonisation rate. If there are fewer meadows in total, there will be fewer occupied patches, and hence fewer sources of colonists. Hence the proportion of the remaining meadows that have butterflies or bumblebees at any one time will be lower. Remove a few more meadows, and it will become lower still. The remaining populations will be few and far between and will begin to become inbred, because they will receive few visitors from outside, and hence extinction rates will begin to climb. Remove too many meadows and you will reach a tipping point, beyond which the number of occupied patches will gently but steadily decline to zero. This is known by biologists as ‘metapopulation collapse'.

Unfortunately it is probably a very common process. Most natural habitats in Europe are now highly fragmented, and the fragments are often not close together. Hence many populations of sedentary habitat specialists – be they snails, butterflies or bumblebees – are separated from one another, with levels of inbreeding slowly increasing. Many might be doomed to extinction by what we have done in the past, so that even if no further habitats are lost we can expect them to slowly, inexorably disappear. This is sometimes described as an ‘extinction debt', and in truth we do not know how many species in the world are in this situation.

Just as it is true that no man is an island, so no habitat island is truly isolated. It cannot survive on its own, for it depends on other islands for sources of colonists, for gene flow to keep populations healthy. Chez Nauche is far more diverse that it was when it was a cereal field, but how many more species might have arrived 100 years ago, when there were many flowery meadows nearby? There are no large blue butterflies, or corncrakes, because these species have largely gone from the landscape – there aren't enough patches left for them to survive. No matter how carefully a nature reserve or habitat patch is managed, it is really only as good as the network of patches of which it is a part.

What we do know is that it is possible to help. We can create new habitat islands, filling in some of the gaps, making the network of patches a little more connected. We can plant new woodlands, link them with new hedgerows, and regenerate flower-rich grasslands such as the meadow at Chez Nauche. It takes time, and we need lots of them, so all the more reason to start now. There is an old Chinese proverb: ‘The best time to plant a tree was twenty years ago. The second-best time is now…'

CHAPTER FIFTEEN

Easter Island

1
August
2013
. Run:
39
mins
38
secs. I was up early this morning; the mist hadn't cleared as I set off and as I ran up the drive one of the barn owls swooped silently past, neither of us seeing each other until we almost collided – a wonderful, ghostly creature. People: only Monsieur Fontaneau junior, inspecting his cows. Dogs:
6
. Butterfly species:
8
, including a large tortoiseshell nectaring on a spear thistle. This butterfly is sadly extinct in the UK, wiped out by the demise of the elms – its larval food plant – at the hands of Dutch elm disease.

I was taught that the human brain was the crowning glory of evolution so far, but I think it's a very poor scheme for survival.

Kurt Vonnegut

Ninety thousand years ago a group of humans living in Africa decided to go for a walk. It was a long and slow walk, fraught with danger. It would take them and their descendants about 80,000 years, but it was perhaps the most significant trek in the Earth's history. For obvious reasons we don't know many of the details – they have been pieced together by archaeologists from fragments of bone and shards of rough stone tools excavated from thousands of sites around the globe. There will no doubt be significant new discoveries and endless arguments about the specifics, but what follows is probably somewhere near correct.

Modern humans – apes belonging to the species
Homo sapiens
– evolved in Africa perhaps 160,000 years ago, at a time when much of Europe, North America and Asia was locked under vast sheets of ice. Our ancestors remained more or less confined to Africa for 70,000 years and then, for reasons at which we can only guess, a group of them left Africa, crossing the mouth of the Red Sea on to the Arabian Peninsula, carrying their stone tools: axes, knives, hammers and arrowheads. They seem to have had a close association with the sea, for they stuck to the coast and spread slowly eastwards, successively occupying the coasts and islands of India, Thailand, Malaysia and Indonesia. It took about 30,000 years before some of them crossed to New Guinea and Australia, approximately 60,000 years ago. Fifty thousand years ago the climate began to warm, and humans were able to spread northwards into the Middle East and Europe. The first humans colonised Britain perhaps 40,000 years ago. At the same time we were also spreading north-east, into Central Asia and China. Twenty-five thousand years ago we had occupied most of the old world, from Britain and Spain in the west to Tasmania and the Bering Straits at the far eastern tip of Siberia. Shortly afterwards a particularly hardy group of humans crossed the eighty kilometres or so from Russia to Alaska, and so colonised the Americas. The climate entered another cold period (the last ‘glacial maximum', in geologists' terms) and buried much of northern Europe, Russia and North America under a vast sheet of ice, pushing us southwards for a while and chasing the new arrivals in America down into the southern states, Central America and beyond. We arrived in Chile perhaps 12,000 years ago, so that about 80,000 years after our ancestors first set out from Africa, all of the Earth's major land masses had been occupied by humans, with the exceptions of inhospitable Greenland and Antarctica.

The final wave of colonisation, of the most remote but habitable places on Earth, took place rather later – perhaps 1,000 years ago, when adventurous Polynesians in dugout canoes chose to sail east from Asia into the unknown vastness of the Pacific. They discovered and colonised New Zealand, the various small archipelagos of Fiji, Samoa and so on, and eventually made it to Hawaii and finally to Easter Island, arguably the most remote inhabited island on Earth.

Homo sapiens
were not the first hominids to leave Africa. Other hominids such as
Homo erectus
and
Homo neanderthalensis
(Neanderthals) had got a huge head-start, spreading throughout much of the old world long before we arrived –
Homo erectus
was found all over Europe and Asia well over one million years ago, while Neanderthals spread throughout Europe perhaps 600,000 years ago. At least twelve different species of ape belonging to the genus
Homo
have so far been described, and it seems very likely that there are many more awaiting discovery. The tiny
Homo floresiensis
from Indonesia, weighing in at about twenty-five kilos and standing just one metre tall, was not discovered until 2003.

The world that early hominids colonised was dominated by large mammals. Following the extinction of the dinosaurs some sixty-five million years ago, widely thought to have been the result of the devastation caused by an asteroid striking the Yucatan peninsula, the few small mammals that survived went on to proliferate. Many new species arose and filled the vacant niches once occupied by dinosaurs, some of them becoming huge. In the Americas this ‘megafauna' included giant sloths, camels and llamas, many species of bison, moose and ox, giant beavers, mammoths and mastodons. These herbivores were predated by some of the most formidable predators to walk the Earth in the last sixty-five million years, including huge two-tonne short-faced bears, a species of lion, several species of sabre-toothed cats and massive dire wolves. In Europe we had woolly mammoths and elephants, aurochs, lions, cave bears, cave hyenas, giant elks, several species of rhinoceros (including the ten-tonne indricotherium, the largest land mammal so far discovered) and much, much more. Each continent had its own magnificent selection of giant, hairy beasts.

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