Tiny dancers

A BBC News crew recently spent some time at the Sanger Institute with Corpus PhD candidate Jonah Walker and his doctoral supervisor Dr Joana Meier learning about the dance of the Australian peacock spiders. But it's not just because the spiders are colourful, charismatic and seemingly quirky – and hence extremely photogenic. Jonah is a member of Joana’s research group, which straddles the Tree of Life Programme at the Wellcome Sanger Institute and the Zoology Department at the University of Cambridge. Jonah says their work "is fundamentally driven by questions about speciation: the process of how new species emerge over time and how we get biological diversity." Joana adds: “We are seeking to explain why some biological lineages have become extremely diverse with many species while other lineages have remained comparatively species-poor, using the peacock spider, amongst other animals, as study organisms.”

Evolved for courtship?

Peacock spiders are an example of a ‘radiation’ – an evolutionary event in which a biological lineage rapidly diversifies into many new species, with the newly formed species each evolving different adaptations. Whereas new species normally take around a million years to evolve, radiations might see new species evolve in just a few thousand years. The peacock spider genus Maratus comprises over 100 species found only in Australia and its males are infamous for the remarkable dances that they perform to attract females, as shown below. Jonah and Joana hope to understand the general principles of species formation by studying the extreme case of the super-diverse peacock spiders.

The females, meanwhile, are dull brown or beige. This extreme sexual dimorphism, together with a lack of observable ecological differentiation between closely-related species, suggests the evolution and radiation of peacock spiders is driven partly by sexual selection – with female spiders selecting mates based on their behaviour or appearance. Jonah says, "Extreme sexual selection is found in many insects and birds, which is why we often see showy males in nature. By and large, females are limited in how many offspring they can reproduce due to their large investment in eggs. Males have no such limit, producing millions of sperm easily. So for a female, it's more important who she mates with rather than how many males she mates with. For the males it just matters that they mate with as many females as possible. So we expect to see showy males and choosy females."

In order to study peacock spiders, the researchers first have to find them. Peacock spiders are tiny – typically only two to eight millimetres across – and Australia is a vast country: truly a needle-in-the-haystack challenge. Besides the scale, the ecological diversity of the spiders is remarkable. "In the interior of Australia you have dry salt lakes and you'll find these spiders on the surface in 45-degree burning heat, dancing away to each other,” says Jonah. “But we’ve also found them in temperate and tropical forests, beaches, dunes, swamps, shrubs, in many places. So the process of finding them is like a game of Pokemon Go but on a sort of continental scale."

Fortunately, Jonah and Joana are part of a large team of Australian, German, US, and UK scientists whose collaboration makes the research possible. Jonah has spent three field seasons travelling the width of Australia multiple times ("four crossings along the bottom, back and forth, back and forth, and then twice across the middle") in the converted campervan of Joseph Schubert. Joseph, a PhD student at Sydney University, had overhauled his van to include a microscope, two-storey sleeping, and four-wheel drive so they could get to the most remote and challenging locations. Along the way, they’ve been joined by a cavalcade of scientific collaborators and local experts. Peacock spiders were launched into the Australian public’s awareness thanks to the early work of the taxonomist Dr Jürgen Otto. As a result, the team benefits from  regional knowledge to find the local peacock spider species, contacting naturalist organisations and peacock spider sighting groups on Facebook and Instagram.

Once found, collecting the spiders is the next step. Some species are "incredibly easy to catch," says Jonah, “while others move like grasshoppers and it can take hours to convert a sighting into a collected specimen. Some people use pooters (clear plastic bug hunters) but my preferred technique is to take a pot with a lid, work out where the spider is going to jump next, and gently encourage it to jump in."

Small spiders, big genomes

The researchers collected several thousand specimens, many of which they brought back to the UK. Most of them were flash frozen with liquid nitrogen, but several hundred were transported alive. "It's phenomenally difficult to rear them," says Jonah, "Hatchlings require very precise humidity, very precise feeding regimens, particular lighting; we haven't quite cracked the code on how to keep them alive in the lab yet."

Once back at the Sanger Institute, the DNA of the specimens is sequenced. "First we have to get a huge amount of DNA out of something that is tiny,” Jonah explains. “Then Sanger’s assembly and curation teams work out how those pieces of DNA fit together like a jigsaw puzzle to make up the animal’s genome. Although they have roughly the same number of genes as most other animals, the peacock spider genomes are huge — about three times more DNA is found in each peacock spider cell than a human cell. That’s because peacock spiders turn out to have unusually long tracks of ‘repetitive DNA’ in between the genes. We used to call this ‘junk DNA’, but increasingly scientists are finding that these non-gene sequences can have important effects on organisms too. All of this means that we have to generate an immense amount of data when sequencing their DNA. The Sanger Institute has an extraordinary supercomputer, so we can do a huge amount of computation very quickly. But even for an Institute which is producing more sequencing data than anywhere else in Europe, it's a lot to ask."

The Sanger Institute’s Tree of Life Programme, which is a leading contributor to the Earth BioGenome Project, uses DNA sequencing to study biodiversity and generate novel insights for nature conservation and society. They aim to generate a gold-standard sequence (known as a ‘reference genome’) for all eukaryotic species, including the peacock spiders. Joana explained: “My group uses a two-pronged approach, whereby we zoom in on specific case studies like the peacock spiders that we investigate in great detail, and we zoom out by sequencing species across the tree of life to understand general principles of evolution. For instance, in a project called Project Psyche led by me and colleagues across Europe, we just reached our first milestone of 1,000 sequenced butterflies and moths found in Europe”.

A dance for all the senses

But genetic sequencing is only one of the tools that Jonah and Joana employ to delve into the evolutionary history of the biosphere. "We need an integrative understanding of the evolution of organisms," says Joana, "and biology benefits from an interdisciplinary and collaborative approach. Our research is grounded in field-based observation and for the peacock spiders we combine this with genomic sequencing, multispectral imaging, and behavioural experiments in the lab."

Male peacock spiders only develop their colouration and patterning once they go through their final moult and become sexually mature; before then they are as camouflaged as the females. The spiders are visually guided and have eight eyes with two eyes in the centre being larger because they actively chase prey rather than building webs. "They have incredible depth perception but struggle to see something in front of them unless it is moving,” Jonah explains. “Once the male spots a female moving, he starts his courtship dance by putting up his colourful abdomen and waving an elongated pair of legs."

What is most remarkable about the male courtship displays is their diversity. Each of the over 100 species has a completely unique dance: a specific suite of colours and patterns on the abdomen; specific leg movements (some species raise one leg at a time, some two, and some four); and specific twists and turns of the body. "Within each species the dance is highly stereotyped, so it appears to be hardwired in by evolution," says Jonah.

Jonah and Joana study both the behaviour and the vision of the spiders to understand what elements are specifically attractive to the females — the brilliant patterns, bright colours, or particular dance moves. But this requires some careful consideration. Peacock spider vision is different from our own, extending into the UV range for instance. Dr Cynthia Tedore, a collaborator at the University of Hamburg, has developed an imaging system which takes 16 images simultaneously. Each image uses a different filter that only allows light of a certain wavelength through. They can then use this data to simulate how the male appears across all of the UV and visible realms of the light spectrum.

 It’s not only the visual component of the peacock spider dances that the researchers are interested in. Previous work has shown that the males also generate vibrations (or ‘songs’) during their dances by tapping their legs on the ground and rubbing their abdomen against their head. These vibrations are detected by the female and they also influence whether the female accepts the male’s advances. Just like the visual traits, each species has a unique vibratory song. So during their last fieldwork trip, Jonah, Joana, and Joseph teamed up with US scientist Professor Damian Elias and recorded the vibrations of every species they found. They used a laser vibrometer which can detect the very fine vibrations produced by males. “We are hoping to see whether species with similar visual traits also produce similar vibrational signals,” says Joana. “This should help us understand how the evolution of these traits is linked to the evolution of new species.”.”

An eye to the future

Understanding the evolutionary origin of species is more than a niche academic interest. Jonah says, "We are trying to understand how we ended up with the diversity we see and there is a conservation interest too. Firstly, if we understand how diversity has arisen in the past, then that might help us understand how we can protect it in the future and also create ecosystems that could facilitate an increase in diversity in the future. But just as importantly, a lot of the work that we do is purely documenting nature. We are currently in the process of describing and naming several species of peacock spiders that we discovered during our fieldwork in Australia, so that there is a record. If there is no record, the organism does not exist to science, and thus cannot be seen by policy. If it's not seen by policy, it cannot be protected."