ARGUABLY the world’s weirdest plant, Welwitschia mirabilis is a tangled mass of shredded, fraying leaves in the Namib desert. For a thousand years, perhaps more, it grows just two long leaves, which creep continuously outwards for many metres, becoming torn and ragged. The plant is a lone survivor; fossils suggest , but all its close relatives are gone.
This evolutionary orphan is a gymnosperm – plants that produce seeds, but not true flowers or fruit. The most familiar today are conifers, a group that includes the longest living organisms on Earth, the bristlecone pines, and the coastal redwood, the world’s tallest trees. But gymnosperms also comprise gnetales (like W. mirabilis), the palm-like cycads and ginkgo, also known as the maidenhair tree. When dinosaurs roamed Earth, they walked among the gymnosperms, which dominated the land. But just as the dinosaur era ended with the Cretaceous, so too did the heyday of the gymnosperms. Today, there are only around 1000 species, mostly conifers. They cling on in a world conquered by a quarter of a million angiosperm species – the flowering plants.
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What went wrong? Until recently, the tale has been that gymnosperms didn’t stand a chance against these beautiful newcomers. Flowers enabled angiosperms to use insects for pollination, boosting their reproductive success and spurring them on to global dominance. But the latest research reveals new twists in this ancient whodunnit. By better understanding why gymnosperms lost out, we may get some clues about their future, too.
Flowers have long been implicated in the gymnosperms’ demise due to timing: when the angiosperms began evolving into many new forms, the gymnosperms went into decline. But we now know that flowers were around for perhaps tens of millions of years before this explosive diversification and march to dominance, which was already taking place in some environments by around 100 million years ago. This is thanks to new techniques for finding and studying mesofossils – tiny fossils that are visible to the naked eye, but need microscopic analysis to reveal their details.
Pioneered by Else Marie Friis at Aarhus University in Denmark, these methods involve carefully sorting, sieving, cleaning and rinsing small fragments of organic material and studying them using electron microscopy and a means of seeing internal details called tomographic imaging. This approach has provided previously unimaginable insights into the relationships and biology of ancient flowering plants, says Peter Crane, president of the Oak Spring Garden Foundation in Virginia.
Crane (favourite gymnosperm: ginkgo) has worked with Friis to analyse many of the earliest known flower fossils. “The abundance of Cretaceous angiosperm flowers that could be obtained using these techniques was a genuine surprise,” he says. In a deposit north of Lisbon, Portugal, they have found some of the , dating to around 125 million years ago, and they already showed some diversity. The flowers were all quite simple and resembled living angiosperm relatives like magnolias and water lilies, but variations in structure – such as the number of petals – suggest that these fossils may represent as many as 30 different species of early angiosperm.
Some researchers believe they may even have found , possibly dating back 164 million years, while attempts to use genetic analyses and other types of modelling to infer the origin of flowering plants have produced even earlier dates. These very early dates are regarded with some scepticism by other botanists, however. But based on the research from Crane, Friis and other researchers, we can conclusively say that flowers themselves arose some time before the angiosperms swept to dominance, suggesting this evolutionary invention wasn’t enough on its own to put paid to the gymnosperms. So what else might explain their downfall?
One of the great advantages of flowers is that they enable angiosperms to attract animal pollinators to streamline their efforts to move pollen around and reproduce. Perhaps the breakthrough moment for angiosperms wasn’t the emergence of their flowers, but when their flowers adapted to become particularly good at manipulating insects.
Once again, new fossils are offering some surprises. They contradict the idea the angiosperms invented insect pollination in the Cretaceous, and show – quite remarkably – that insects have been pollinating gymnosperms since the preceding period, the Jurassic, before many experts think flowers even existed.
Today, the gymnosperms that many of us are most familiar with – the conifers and ginkgo – are wind pollinated. But hundreds of cycads and gnetales, including W. mirabilis, are pollinated by insects. Until recently, however, it was unclear whether this reflected an ancient relationship between gymnosperms and pollinators, or a more recent occurrence.
“Twenty years ago, we were dealing with just a few isolated glimpses,” says Michael Engel at the University of Kansas (favourite gymnosperm: cycads). The lack of insect fossils from the Cretaceous, particularly the early Cretaceous and the Jurassic, left researchers with little to go on. But since then, “it’s like the Earth has been vomiting up material”, says Engel, thanks to advances in finding fossil deposits from this time, particularly amber. As a result, the Jurassic and Cretaceous have gone from being lamentably fossil-poor to one of the best-known windows of time, he says.
This abundance has enabled Engel and others to finally catch ancient gymnosperm pollinators red-handed. In 2018, he and his colleagues published , mid-Cretaceous beetle preserved in amber with cycad pollen. Like its living relatives, the beetle had various specialised body parts that could carry and store pollen, including a cavity in its mandible. “It has specialisations for transporting pollen, and the pollen is not uniformly distributed in the amber – there is a concentration of it around these mouthparts,” says Engel, whose study estimates that this beetle-cycad relationship could have emerged in the Jurassic. And this wasn’t a unique plant-insect relationship either – a , including and flies, have also been implicated in pollinating a range of different types of gymnosperm in the Jurassic and early-to-mid-Cretaceous.
Powerful pollinators
Simply harnessing insects for reproduction can’t, therefore, be the secret to flowering plants’ success. But the timing of the rapid boom in flowering plant evolution might nevertheless provide a clue, since it coincides with the emergence of some particularly good pollinators. The fossil record for bees is still poor, but it is thought that, some time in the mid-Cretaceous, some carnivorous wasps became vegetarian, started eating pollen and began diversifying into thousands of bee species. “I would say bees are certainly a very important player,” says Engel.
The emergence of bees also coincided with an explosion in the diversity of a group of moths and butterflies, known as the ditrysia. “They’re incredible pollinators, and they’re tightly associated with that same time period when bees are taking off,” says Engel. Today, we have some 20,000 species of bees, but more than 150,000 butterflies and moths, almost all of which belong to the ditrysia group.
Thanks to the colours, odours and nectar of their flowers, angiosperms were able to form tight relationships with these newer, highly effective pollinators. “All of this is far more effective than anything that gymnosperms had [developed],” says Engel. “So now you’ve got a group that’s really predominantly taking advantage of animal vectors.”
Case closed, you might think: the bees’ and butterflies’ preferences for flowers drove the angiosperms’ rise and diversification and – as a consequence – the fall of the gymnosperms. But a few obvious counter-examples prevent such a neat conclusion. “Think of the grass family,” says Patrick Herendeen at the Chicago Botanic Garden (favourite gymnosperm: ginkgo). “Grasses are one of the most diverse families of flowering plants and they’re wind pollinated. So there’s something else going on there that has allowed the grasses to diversify to the great extent that they have.”
Herendeen agrees that animal pollination is “certainly a big factor” in the angiosperms’ success, but suggests other aspects of the angiosperm life cycle – such as the speed of fertilisation and seed formation that take place after pollination – could have also fuelled the diversification of flowering plants.
“The time that it takes to go from flowering to production of mature viable seeds is very short in most angiosperms,” he says. “The gymnosperm group, they have quite a slow reproductive cycle. Pollination to seed maturation takes an incredibly long time, and then even when the seeds fall from the plant, they’re not mature.”
Gigantic genomes
The evolutionary ramifications of this became clear in 2017, in a study by Amanda De La Torre at Northern Arizona University and her colleagues, which compared tens of thousands of points across the genomes of gymnosperms and angiosperms. They found that, just as some gymnosperms today , with the ginkgo, dawn redwood and Wollemi pine all bearing a striking resemblance to ancient fossil remains, gymnosperms also appear remarkably unchanged at the molecular level. Many gymnosperm genes in today’s plants look identical to their counterparts from millions of years ago, whereas angiosperm genes have accumulated mutations far more quickly.
Mutation is a double-edged sword – it provides new opportunities for evolutionary innovation, but it can also damage or harm an organism’s basic functioning. “Angiosperms are changing way faster than gymnosperms. They may have a lot of deleterious mutations, but they also may have a lot of advantageous mutations,” says De La Torre (favourite gymnosperm: Douglas fir). This may have enabled angiosperms to colonise geographical areas where gymnosperms weren’t able to survive, she says.
Besides the effects of their slow reproduction, gymnosperms also have to contend with the sheer size of their genomes, which can be as much as seven times as large as a human genome. De La Torre’s research suggests that this is also linked to gymnosperms’ slow mutation rate. Indeed, across much of life on Earth, larger genomes have often been found to evolve more slowly.
To make matters worse, large genomes also directly affect the physiology of an organism’s cells, setting a limit for the smallest size a cell can be. This can have a profound influence on a plant’s anatomy and functioning, according to a recent study comparing the genome size and anatomy of 289 angiosperms and 53 gymnosperms.
The analysis revealed that angiosperms in the Cretaceous period. Adam Roddy at Florida International University and his colleagues argue that this enabled them to have smaller cells, making it possible to pack their leaves with more veins and more stomatal pores for bringing in carbon dioxide for photosynthesis. “Smaller genomes allow for smaller cells and higher rates of photosynthesis, higher rates of growth,” says Roddy (favourite gymnosperm: Araucaria, the monkey puzzle trees). “You can grow faster and outcompete your neighbours.” The gymnosperms were unable to do the same.
This builds a picture of the angiosperms’ formidable armoury – they could grow faster, evolve more quickly and use their innovative new flowers to reproduce very effectively via newly evolved bees, butterflies and moths that were undergoing their own rapid diversifications. It is easy to see how this could have led the angiosperms to suddenly evolve into a large number of new species.
Detailed modelling looking at the suggests this diversification of angiosperms was the most important factor in the increased extinction rate of gymnosperms that began in the mid-Cretaceous. “Our work suggests that the diversity of angiosperms contributed to increase the extinction of conifers,” says Fabien Condamine at the French National Centre for Scientific Research (favourite gymnosperm: Araucaria). This was particularly evident in tropical regions, where conifers once flourished until the angiosperms took over.
Condamine and his colleagues’ work also suggests that global cooling around 34 million years ago may have played a secondary role. “We see a lot of extinction occurred at that time. It is possible that conifers were slow to adapt to this cooling trend,” says Condamine.
Sadly, Condamine’s work found that extinction rates for conifers have remained high ever since the mid-Cretaceous. According to researchers at Royal Botanic Gardens, Kew, in London, 40 per cent of gymnosperm species are , making them one of the most threatened groups on Earth. We now know that slow-evolving gymnosperms don’t appear to cope well with times of rapid climate change, which raises the alarm for how these plants will fare over the next century.
But we shouldn’t write off gymnosperms as evolutionary losers. “I guess I’ve become a little defensive of the gymnosperms,” says Roddy. Many are doing fine, he says, and they are in ecological settings in which their strategies for life seem to be working.
Today, the most threatened gymnosperm species tend to be those that have clung on in tropical regions. But many gymnosperms have now adapted to life in colder environments and conifers dominate many temperate and high-latitude forests in North America, Europe and Asia.
They may be slow to grow, reproduce and evolve, but gymnosperms have been on this planet for three times as long as their flowering plant relatives. It will be hundreds of millions of years before we know whether the flashier flowering plants are capable of such staying power.
