Evolutionary dead ends

By Athayde Tonhasca

In 1842, the Darwin family – Charles, his wife Emma, and their two children William and Anne – moved to Down House in the village of Downe, England. The Darwin patriarch, who had travelled the world aboard H.M.S. Beagle (1831–1836), would spend the remaining 40 years of his life in quiet isolation at home because of ill-health. Darwin’s condition (whose origin still puzzles scholars) did not slow him down; he embarked on several projects such as monographs on coral reefs and barnacles, and of course overseeing the publication of On the Origin of Species. But Darwin spent most of his time working with plants, which are convenient study subjects for someone with a sedentary life-style. Assisted by gardeners and occasionally his children, Darwin observed and experimented with cabbage, foxglove, hibiscus, orchids, peas, tobacco, violets and many other species in his garden and glasshouse.

Darwin’s glasshouse at Down House, where he conducted many experiments © Tony Corsini, Wikimedia Commons.

Among various major contributions to botany (detailed by Barrett, 2010), Darwin documented the importance of cross-fertilisation (i.e., the transfer of pollen between different plants) for producing healthy offspring. Darwin, ever meticulous about supporting his theories with data, amassed eleven years of continuous observations to highlight the superiority of cross-fertilisation over self-fertilisation, i.e., the transfer of pollen within the same flower or between different flowers on the same plant. 

Methods of transferring pollen from the male anthers to the female stigma © Bartz/Stockmar/Ziyal – Insect Atlas, Wikimedia Commons.

Indeed, the great majority of flowering plants predominantly or exclusively outcross – that is, they mate with other individuals – even though they could easily self-fertilise because they are hermaphroditic (their flowers contain both male and female sexual organs). In fact, numerous flowers have mechanisms to avoid self-fertilisation. At best, many self-pollinated species (or ‘selfers’) exhibit mixed mating systems.

The bee orchid (Ophrys apifera). Despite its name, this orchid is mostly a selfer in northern Europe. In the Mediterranean, where this orchid is more abundant, its flowers are pollinated by bees © Bernard Dupont, Wikimedia Commons.

Self-pollination has some advantages: it helps to preserve desirable parental characteristics when a plant is well adapted to its environment. Because selfers do not depend on pollen carriers, they can colonise new habitats with a handful of individuals. Selfers do not have to spend energy on nectar, scents, or substantial quantities of pollen. Self-pollination is useful to farmers, as the genetic identity of a variety or cultivar is easily maintained, without requiring repeated selection of desirable features.

Comparing self-fertilised and crossed seedlings of common toadflax (Linaria vulgaris) in his garden prompted Darwin to investigate the effects of cross-fertilisation (Thompson, 2018) © Tony Atkin, Wikimedia Commons.

Self-pollination sounds like a convenient and rational lifestyle, but there are catches, and they are considerable. Selfers’ limited genetic variability makes them vulnerable to environmental changes; a hitherto well-adapted population can be driven to extinction if no individuals are adapted to novel conditions – and changes are inevitable, given enough time. Selfers are also particularly susceptible to inbreeding depression; if the population is homogeneous, genetic defects cannot be weeded out by genetic recombination.

Taking into consideration the long-term hazards of selfing, it seems paradoxical that 10 to 15% of all flowering plants from many taxonomic groups made the transition from outcrossing to full self-fertilisation. Darwin proposed an explanation for this puzzle: cross-pollinated species would turn to self-fertilisation when pollinators or potential mates become scarce. In other words, self-fertilisation assures survival when outcrossing becomes inviable. Darwin’s hypothesis, currently known as the ‘reproductive assurance hypothesis’, continues to be the most accepted explanation for the evolution of self-fertilisation.

Remarkably, researchers were able to quickly induce the transition from cross-pollination to self-pollination in the common large monkey flower (Erythranthe guttata, previously known as Mimulus guttatus) by preventing plants’ contact with pollinators (e.g., Busch et al., 2022). Monkey flowers kept in a glasshouse with no pollinators for five generations increased the production of selfing seeds and showed a reduction in the stigma to anther distance – this feature, known as herkogamy, is one of the indicators of ‘selfing syndrome’: the greater the distance between stigma and anther, the greater the likelihood of the stigma receiving external pollen, thus the lower the chance of self-pollination. After nine generations, plants experienced a significant reduction of genetic variability. Monkey flowers kept in another glasshouse with free access to the common eastern bumble bee (Bombus impatiens), one of the plant’s main pollinators, underwent none of these changes.

L: The common large monkey flower, a native to western North America. Its wide corolla and landing platform are convenient for its main pollinators, bumble bees © Rosser1954, Wikimedia Commons. R: Diagram of a large monkey flower with the upper corolla removed to show the reproductive structures © Bodbyl-Roels & Kelly, 2011.
A common eastern bumble bee; its absence induces selfing in large monkey flowers © U.S. Geological Survey Bee Inventory and Monitoring Lab.

What do these observations of the monkey flower tell us? For one thing, they are cautionary tales about the risk of losing pollinators. A variety of human disturbances such as agriculture intensification, loss of habitats and diseases have caused a decline of some insect populations, including pollinators. A scarcity of flower visitors may threaten pollination services directly, or induce some plants to adapt quickly and become self-pollinated. Adaptation sounds good, but selfers’ lower genetic diversity and reduced capacity to adjust to environmental vicissitudes make them vulnerable to extinction.

The renowned botanist and geneticist G. Ledyard Stebbins (1906-2000) suggested that selfing is an evolutionary dead end: it is advantageous in the short term but harmful in the long run. And because the transition from outcrossing to selfing is irreversible, according to Dollo’s Law (structures that are lost are unlikely to be regained in the same form in which they existed in their ancestors), self-fertilization ends up in irretrievable tears. And the monkey flower has shown that it all may happen before we notice it.  

Loss of pollinators could be the end of the line for plant species forced into self-pollination © Vaikoovery, Wikimedia Commons.

A hard flower to crack

By Athayde Tonhasca

Brazil nuts are high up in the list of superfoods, a gimmicky but highly profitable market. For some internet gurus, the nuts protect you against inflammation, heart disease, diabetes and cancer; and, inescapably as superfoods go, they are loaded with ‘antioxidants that fight free radicals’ – a scientifically baseless but commercially catchy label. Hype aside, Brazil nuts are highly nutritious: they are loaded with proteins, carbohydrates, unsaturated lipids, vitamins and essential minerals such as calcium, magnesium, phosphorus and potassium. But their main claim to fame is to be one of the best sources of selenium, an essential element for a range of metabolic processes in our bodies. These nuts have their detractors because of the unlikely risk of selenium poisoning for those who over-indulge in them, and the danger posed by aflatoxins (carcinogens produced by certain fungi) when the nuts are not stored properly. The healthy aspects of Brazil nuts are clearly winning over the popular perception because the European and American markets keep growing steadily. Which is good news for the main nut producers Bolivia (the world’s major exporter), Brazil and Peru.

Assorted nuts, essential while watching a match on the telly © Melchoir, Wikimedia Commons.

The nuts are in fact seeds extracted from the hard, coconut-like fruits produced by the Brazil nut tree (Bertholletia excelsa). Named excelsa (high, exalted, lofty) by naturalists and explorers Alexander von Humboldt and Aimé Bonpland, this is one of the tallest trees in the Amazon region. Some individuals reach heights of 30 to 50 m, with trunks of 1 to 2 m in diameter – up to 5 m in older specimens. And they can live long lives: radiocarbon dating has identified some 800- and 1000-year-old trees (Camargo et al., 1994).

Brazil nuts are gathered from fruits fallen to the forest floor during the rainy season. The work, carried out by native people and small farmers, has one serious risk: the thick-walled fruit of the Brazil nut tree is 10-15 cm in diameter and weighs on average 750 g. A fruit of this size falling from about 7 m generates sufficient kinetic energy to fracture a skull and cause severe to fatal injuries (Ideta et al., 2021).

A Brazil nut fruit and seeds in their shells, and seeds ready for the market © P.S. Sena and Quadell, Wikimedia Commons.

Brazil nuts are harvested almost entirely from wild trees because tree cultivation has been largely unsuccessful. One of the reasons for the failure to turn the tree into a farm commodity is its pollination requirements.

The Brazil nut tree reproduces by cross-fertilisation, but its flower is not the run-of-the-mill, pollinator-friendly structure found in most plants. It has a curled extension – called a ligule – that forms a hood over the petals, which are pressed together like an inverted cup. Ligule and petals create a chamber that conceals stamens, stigma, and the nectaries. To access the nectar, an insect has to squeeze itself between the ligule and the tightly packed petals. If successful, the visitor may come out dusted with pollen and transfer it to another flower.

The inflorescence of a Brazil nut tree © Scott Mori, The New York Botanical Garden, Lecythidaceae – the Brazil nut family.

The flowers of the Brazil nut tree receive many visitors, including hummingbirds, moths, butterflies, beetles, and several bees. But getting into a flower for its nectar is not for the nimble or weak; only the largest and strongest bees can lift the ligule to reach the reproductive organs.  This select heavy-weight club includes bumble bees (Bombus spp.), Centris spp., Epicharis spp., orchid bees (Eulaema spp.), and carpenter bees (Xylocopa spp.). 

An E. meriana orchid bee (L) and a large carpenter bee (X. mexicanorum), two of the robust bees capable of handling a Brazil nut tree flower © Insects Unlocked, Wikimedia Commons.

In the central Amazon rainforest, the orchid bee E. mocsaryi and carpenter bee X. frontalis are especially important Brazil nut tree pollinators because of their abundance and frequency of flower visitations (Cavalcante et al., 2012). Watch X. frontalis hard at work. 

An E. mocsaryi orchid bee forces itself between the ligule and the tightly packed petals of flower of the Brazil nut tree © Cavalcante et al., Wikimedia Commons.

The large bees that pollinate the Brazil nut tree can fly long distances, which is important for maintaining its genetic diversity: trees typically grow in groups of individuals that are isolated from each other in the forest. These bees are solitary or semi-social, and none of them have been domesticated; so their survival depends on the natural habitats that supply nesting sites, food – one type of tree alone will not provide for the whole season – and other resources such as orchid fragrances, which are collected by male orchid bees.  

Other characters play an important part in the life of a Brazil nut tree: rodents. The fruit capsule is too hard for most animals that could be interested in the nutritious seeds – but not to agoutis (Dasyprocta spp.). Thanks to their powerful teeth, they can gnaw their way to the seeds. Sometimes an agouti can’t eat all the seeds at once, so the prudent animal takes them some distance away (up to 20 m) and buries them as a food reserve for leaner times. But it so happens that the agouti’s memory is not the sharpest; it often forgets the way back to the food cache. Or the agouti itself may become a meal for a large cat before returning to its seeds. Either way, the buried seeds germinate. This unintentional planting by agoutis, pacas (Cuniculus spp.) and the southern Amazon red squirrel (Sciurus spadiceus) is the only route to seed dispersal for the Brazil nut tree, thus is vital for its survival. Follow the exploits of a forgetful agouti in the forest.

A red-rumped agouti (Dasyprocta leporina) © Alastair Rae, Wikimedia Commons.

As one can imagine, these required interactions with bees and rodents don’t bode well for the future of the Brazilian nut tree. Amazonian ecosystems have been eroded away by the relentless march of deforestation and land conversion to agriculture and pastures. To make things worse for the tree, its wood is highly valuable (its felling is illegal, but that doesn’t stop illegal loggers). One of the consequences of the devastation is the increasing scarcity of Brazil nuts in Brazil, which helps explain why Bolivia took the lead as the main exporter. 

We may take the hard-nosed view that we can’t do anything about the plight of the Brazil nut tree, but that’s not quite right. One could be inquisitive and demanding about the origin of a nice piece of hardwood furniture for sale, or the juicy steak in a restaurant or supermarket freezer (much of exported South American beef comes from deforested areas). Or we could accept a life without Brazil nuts: after all, to us they are just comfort food. But the tree’s demise could be a portent. In the 1980s, doomsday prophet Paul Ehrlich and his wife Anne Ehrlich famously compared species’ roles in an ecosystem to rivets in an aeroplane’s wing. Aircraft manufacturers use more rivets than necessary to affix the wings, so removing a few of them would make little difference. But if they continue to be taken away, at some point a critical rivet is lost, and the aeroplane will crash. Similarly, how many species can you lose before an ecosystem fails? We don’t have an answer for that, or even know whether the Ehrlichs’ model is realistic. The eventual loss of the Brazil nut tree could be just one redundant rivet popped out of the body of biodiversity; or it could be a warning of bad things to come to bees, agoutis, the forest and its peoples, and, at the end of the queue, to us, sophisticated Brazil nut munchers. 

The Brazil nut tree is the symbol of the Amazon Forest. Its size makes it difficult to capture it whole in a photo © upper left: My Favorite Pet Sitter; lower left: mauroguanandi; rigth: Edsongrandisoli, Wikimedia Commons.