About Wayne Maddison

I am a biologist at the Beaty Biodiversity Museum (University of British Columbia), studying spider diversity and evolution. My specialty is jumping spiders (Salticidae).

Portraits of Singapore

Some day, when I can play the violin and have the tangle of cables behind my desk dusted and organized, I’ll learn how to paint in oils, and I’ll do formal posed portraits of jumping spiders in book-filled studies or luxurious garden backdrops. In the meantime here is the unusually proportioned Cocalus, from Singapore.

Cocalus female. Note the long palps, the low position of the lateral eyes, and the big posterior median eyes. She’s a spartaeine.

And here are, respectively (from top left, across and down), the alien Viciria, the grumpy Pancorius, the direct Parabathippus, the fabulous Chrysilla, the spooky Portia, and the self-assured Hyllus.

Portraits of Singaporean jumping spiders

Advertisements

Singaporean gold

The jumping spider tribe Chrysillini takes its name from the genus Chrysilla, whose name means, more or less, the little golden one. Gold promises brilliance, and Chrysilla is more than brilliant gold — it’s a jewel of many colours. Here is a stunning male we got on Pulau Ubin in Singapore:

Chrysilla male from Singapore

The chrysillines are quite common across Eurasia and Africa, and are a target of our collecting in Singapore. We found many species of chrysillines, including species of Siler, Cosmophasis, Menemerus, Epocilla, Pseudicius (s. lat.), Phintella, and Phintelloides. Here are gloriously shiny males of the latter two genera

Males of Phintella and Phintelloides

Common in some places in Singapore are charming little chrysillines that I think belong to Helicius. Here are females of two different species that we think are closely related, because there respective males are quite similar.

Females of two species that I think are Helicius

As with the Plexippina, the Chrysillini include only a few species in the Americas, and so it’s a branch of the family I can’t find in my backyard.

Formalities of the Plexippina

A bit of formality: The traditional taxonomic classification has families, genera, and species. Sometimes, a family is divided into subfamilies, and the subfamilies into tribes. Within the jumping spider tribe Plexippini, there are even subtribes, one of which is the Plexippina. This species-rich group is ubiquitous in Eurasia and Africa.

The Plexippina deserve a bit of formality, as the males of one of the most familiar species, Plexippus paykulli, wears a sharp tuxedo of black and white. In Singapore we found plenty of other species of plexippines, most with more relaxed — or outrageous — attire. Among the most outrageous is the very large jelly-green Artabrus:

Adult male Artabrus, a large green member of the Plexippini.

I had never seen a living Artabrus before, and I was thrilled. Contrasting against its greenness were two orange-and-black species of Pancorius:

Two orange-and-black Pancorius species

A big and a little Evarcha from Pulau Ubin were of special interest for the colour vision study, as we suspect some African Evarcha can distinguish red:

Two species of Evarcha, to the same scale, both males.

In the Americas we have only two native species of Plexippini, both Evarcha, and so it’s quite a treat to see so much plexippine diversity. Here are a few of the other plexippines we found in Singapore.

A sampling of plexippines from Singapore

A Wall of Neon Lites: Update to “Apologies to a Spider”

A couple of weeks ago I blogged about my dismay in losing a special specimen, a tiny tiny striped jumping spider that escaped in my hotel room. I regretted losing the chance to make the species better known. Well, we have an update.

A few days before leaving Singapore, we went back to the same area to look for more. After several frustrating hours, I found another specimen of the tiny striped thing. Not just one, but three, in the same shake of some ferns. Over the next few hours, we homed in on the habitat, and could predictably find more. This is one on my beating sheet:

My finger pointing to an adult male Neon sumatranus on my beating sheet.

Here’s where they live. In the forest are occasional small sunny clearings, possibly where a tree has fallen, and these clearings are choked with ferns. The ferns rise upward along the trees facing the clearing, forming walls of lush fern-ness. Underneath, in the tangle of stems at the base of these rising ferns, is moist leaf litter suspended just above the ground. The tiny striped spiders seem abundant in that leaf litter, and at least in the morning, up among the green ferns themselves.

Where Neon sumatranus lives

Kiran and I found several males and several females, and we knew we had everything that we needed to characterize them. As soon as we got back to the lab, I looked at a male under the microscope to figure out what it was, and got a surprise: we don’t need to do the basic characterization, because it’s already been done. It’s a known species.

 

Not only is the species known, but it’s closely related to a species I grew up with in Canada, Neon nelli. The tiny striped thing is Neon sumatranus, described by Dmitri Logunov in 1998, from Sumatra and Borneo. How could I not have recognized it as a Neon? Well, all of the Neon species I’d seen in the past are “bigger” (i.e. 2.5 mm instead of 1.5 mm), and with characteristic black and brown colours. Neon sumatranus is quite unusual among Neon for its super small size and its stripes.

The other thing that kept Neon from my mind is that I think of them as temperate zone creatures, being best described from Europe, northern Asia, and North America. This is not the correct way to think about them, however, as phylogenetic evidence and unpublished explorations suggest that Neon is actually an Australian group that has dispersed around the globe. So, finding it in southeast Asia shouldn’t have been a surprise to me.

I’m not disappointed that it is a known species, and that I was needlessly upset at losing the first male specimen. That upset provoked me to introspect, which was useful. And while it was known, it was barely known, as is the case for most of the world’s species. Now, we can learn more about it. And, they are *so cute*. Here’s a video of a male. Remember he’s 1.4 mm long.

As one of the smallest jumping spiders, it challenges us to explain how it can pack the sophisticated visual system of salticids into such a small head. Vision biologists want to know the answers to such questions. Now that we know how to find Neon sumatranus predictably in the ferns of Singapore, we have a chance to study their tiny tiny eyes.

In the Neighbourhood of Nannenines

We’re all used to biodiversity being localized — kangaroos in Australia, tigers in Asia — but the degree of localization varies from group to group. A broader group of species may be distributed across the world (e.g. bats), even though individually each of its distinct species might have a limited range. In the case of jumping spiders, some broader groups are quite restricted. Nannenines, for instance, are only in southeast Asia, the thiratoscirtines only in Africa.

Singapore, and southeast Asia in general, is the land of nannenines. That mouthful of Ns refers to a group of species of little jumping spiders most of whom hop on the leaf litter of forests. They hold a special place in my heart, for I met them on my memorable first trip to Asia in 2005. Back in Singapore 14 years later, I was pleased to see some familiar faces. Here are two, Idastrandia and Nannenus, shown at the same scale.

Males of Idastrandia orientalis (left) and Nannenus syrphus (right), to same scale. 

From my previous sampling, there remained some puzzles. For example, in 2005 I’d found two types of male Nannenus and two types of females, but I couldn’t figure out which male matched with which female. (I could have seen which males mated with which females, but that type of behavioural experiment requires more specimens and time than I had.) Now I think I’ve figured it out by getting paired types in the same patches of leaf litter. This seems to be the pairing.

Nannenus species A (left) and B (right), with males on top and females on bottom. Yes, they look a lot alike.

Nannenines are very poorly known; there are many species that I’ve collected, but only a few have been described scientifically. Perhaps they haven’t been as well collected as other salticids because they are hidden in the dark forests.

I suspect their preference for dark humid places is also the reason they are localized to southeast Asia. For their ancestors, finding a moist and shaded path between southeast Asia and the African rainforests, for instance, was rather difficult, with habitats inhospitable to them — deserts and savannahs — intervening. Reciprocally, the thiratoscirtines of Africa are mostly isolated to the shaded rainforests, and are not known from Asia. In contrast, groups of jumping spiders that live in open sunny habitats, like the chrysillines and plexippines, are widespread across Africa, Europe, and all corners of Asia. If you want to find the unique salticids of an area, go to the humid darkness.

Convergence on Colour

I’d mentioned in a post earlier today that there was a second motivation for me to come to Singapore beyond basic biodiversity discovery. We are here to survey spiders for their colour vision, working with Li Daiqin of the National University of Singapore. I’ve visited Daiqin before, in 2005, when we worked together sampling jumping spiders. Here he is, 14 years ago, arranging our field work as we travelled by boat to Palau Ubin.

Li Daiqin in 2005, going to Palau Ubin for field work.

Daiqin is a well known spider biologist studying their behaviour, physiology, and ecology. In other words, how they function as organisms. Normally, these aren’t topics I work on, but we can understand evolution more completely by studying function (Daiqin’s expertise) in multiple species and mapping it on the evolutionary tree (my expertise). Thus my second motivation in coming to Singapore is to help study the evolution of how jumping spiders work, using diverse representatives from the Singaporean fauna.

In the last paragraph I shouldn’t have used the singular pronoun “I”, because really I am just part of a large team that is coming to Singapore this month to study jumping spiders’ ability to see colours. The team, led by Nate Morehouse of the University of Cincinnati, chose Singapore as a perfect blend of accessible diversity and world-class science. I’ve explained in a previous post why spider colour vision so interesting that we have formed an international collaboration to study it.

The five spider biologists converging on Singapore are Nate Morehouse from the University of Cincinnati and David Outomuro and Jenny Sung from his lab, and myself from the University of British Columbia and Kiran Marathe from my lab — representing in total five different countries (USA, Spain, China, Canada, and India).

And so, for the next two weeks we’ll be in the forests, mangroves, swamps and beaches of Singapore to look for diverse jumping spiders to study for their colour vision. We also look forward to the hawkers’ markets, the beautiful cityscape, and the friendly people of Singapore.

Red in a spider’s eyes

You probably never imagined the world through a spider’s eyes, but if you did, chances are you’d wonder how they consolidate the signals from eight different eyes. In that, however, they may not be as different from you as you might expect, because after all, we humans have to blend signals from parts of our eye that see differently: the peripheral vision that is better at low resolution motion detection, and our central vision that is better at high resolution colour images. Different animals have visual systems that differ in details, and yet perhaps their evolution responds to consistent selective pressures, or is constrained to find consistent solutions. And so, comparative biologists study many species to see if we can find the rules of visual evolution.

To better understand how vision evolves, a group of biologists led by Nate Morehouse of the University of Cincinnati have turned to jumping spiders (“salticids”), and in particular how they see colour. Jumping spiders have exquisite eyesight — as you can tell by watching a jumping spider watch the world — and yet it was an open question as to how well they could see colour. Studies suggested that some (most?) jumping spiders are as colour-blind as a dog, unable to distinguish red from green.

However, some species of jumping spider gave us a strong hint that they can see and distinguish red: their males have fancy plumes and scales and spurs full of colour, including red. These include the now-famous peacock spiders of Australia (Maratus) and the paradise spiders of North America (Habronattus). Here’s the wonderful Habronattus americanus.

Male Habronattus americanus

That the males display these ornaments to the females during courtship suggests that these females can likely distinguish red.

After Daniel Zurek, Morehouse and colleagues discovered a ruby-red filter in the eyes of Habronattus that gave them the ability to distinguish red, Nate pulled together an international team to see whether and how other jumping spiders could see red, including Megan Porter (University of Hawaii), Lisa Taylor (University of Florida), and myself.

What motivates us is this simple observation: There are only a few lineages of salticids with red male courtship ornaments, and those are scattered in isolated pockets on the evolutionary tree. Most groups of jumping spiders do not obviously (to our eyes!) use red in their male courtship ornaments, and so we might surmise they lack the ability to distinguish red. The scattered distribution of red ornaments hints that the ability to see red has evolved several times independently.

Independent evolution of a similar trait is magic to an evolutionary biologist, because it offers the possibility of discovering the rules of evolution: Under what circumstances does red-distinguishing vision evolve, typically? What are the consequences of evolving this ability?

Salticids give us a special opportunity to answer these questions. Our preliminary assessment is that red-distinguishing vision has evolved multiple times independently in jumping spiders, perhaps more than a half dozen times. That’s a remarkably large number for a group of terrestrial animals that has diversified in only the last 60 million years. And so, our team will survey across the evolutionary tree of jumping spiders to find out what colours their retinae are sensitive to, what light environments they live in, and how it affects their lives.

Apologies to a spider

Imagine holding in your hand, or in your thoughts, something so precious that you are no longer in peaceful control. Your hands may shake; your heart might race. I expect you’ve had that feeling, and worried that you might be more likely to fumble it precisely because the thing is so precious. This just happened to me with a spider: I fumbled it. As I’ve been mourning the loss, I have been surprised at why it hurts so much. I feel I’ve hurt a whole species of spider.

The spider to whom I’m apologizing.

Yesterday, Kiran and I were in Singapore’s wondrous Bukit Timah Nature Reserve, working to discover what jumping spiders are there. I was looking for them using a beat sheet — a square of fabric stretched with tent poles, held beneath vegetation. I shook a tangle of vines and dead leaves and sticks and living plants, and onto the sheet fell debris of various kinds, along with some little animals: insects, spiders, and crustaceans.

There in the middle were two tiny jumping spiders, so tiny that they looked wrong. They would have been small even if they were babies, but they seemed to have the proportions and movements of more mature spiders, which made them seem even smaller, Lilliputian. Even though I assumed they were juveniles, they intrigued me enough that I collected them into a vial, to examine when I came back to civilization. Normally, I don’t collect immature spiders, as they are too difficult to identify. I promptly forgot about them and continued the sampling.

Last night, back in my room, I looked at them as I sorted through the vials of spiders collected, and was shocked to see they were both adults, a male and female. The male is about 1.3 mm long, the female about 1.6 mm, measured from photos of the spiders alive. This puts them among the smallest known adult jumping spiders. Here’s the male on a Singaporean coin.

New tiny jumping spider, on Singaporean coin. This is an adult male.

I’d never seen any spiders like this before. Those of us who explore biodiversity in the wild usually don’t know that something is new until examining it carefully (e.g. under a microscope) and consulting the literature. But these I immediately knew were likely new species, and perhaps even so distinct that we would likely call them a new genus. Here are more photos of the male:

The tiny male.

And here are photos of the female:

The tiny female.

With their size and compact body, they don’t look familiar at all. I can’t think of anything already known from Asia that they could be. I suspect these are the first two collected specimens of a new genus of jumping spider. I don’t even know what general group they belong to — they could be euophryines, or hasariines, or something else. (Salticid geeks: the palps are not big, nor do they look complex enough to be eupoines.)

My heart raced. I started to think: Oh, what if they die overnight (unlikely, but possible if they are very sensitive), and I don’t get a chance to take a photo. So I decided to take photos, even though I was really tired. I carefully prepared a safe open space on the white table to take the photos, so that even if they started hopping and running, I could catch them before they got away. After taking photos, I thought, Oh, I should give them water, in case they need it. Even more tired at this point, I carried the male’s vial to the sink, opened the cork, dipped my forceps into the tap’s water, and dabbed it against the inside wall of the vial.

At that moment the tiny male, unexpectedly, jumped onto the forceps and started running up it. Instantly I could see the danger — I couldn’t close the vial with the forceps, but taking out the forceps would bring him out above the sink. My instinct to get him to a safe place kicked in, so I rushed the three meters to the white table. Three meters over a black and dark brown floor in a poorly lit room with a 1.3 mm spider making a mad dash for escape.

He succeeded. When I got to the table, he wasn’t anywhere to be seen. Fruitless searching with a head lamp came up empty. I doubt he’ll find his way back to his habitat.

His escape was followed by many thoughts, some of them about how impatient and careless I had been — should have left them until the morning; should have brought the water to the table; could have let him fall on the sink — but others about why it hurt so much. Of course, it hurt because I felt that I was stupid and a failure, but that wasn’t the dominant flavour of the pain. It was more about losing knowledge.

To learn about this species, we still have the female specimen to study, but there are two reasons the male mattered. First, a second specimen gives us some leeway for how we study them. Second, males give us extra features to look at that are often the quickest ways to identify the species and understand what it’s related to. With a male, I could know quickly what major group it belongs to just by a glance under a microscope, while we may need to get genetic data if we have only the female, and for that we’d have to sacrifice some of the body of this very tiny female. And so, with his loss we lost knowledge, about the males of his species, about the species itself.

As I brooded, I realized that I didn’t mind much my own personal loss of knowledge. Rather, I felt I have left a burden to other arachnologists to go out and search the forest for a 1.3 mm long jumping spider.

Even more importantly, by losing the male I diminished an opportunity to make the species known, which I see as a vital gift to the species. Literally, vital. If we never knew it existed, it could not factor into any of our conservation decisions. Each species is a small voice calling us to make good choices on its behalf. There may be many species, but every voice counts. We biodiversity discoverers do feel that we serve the species we discover. We introduce them to the other humans, in hopes that appreciation develops.

And so, mysterious Singaporean species of tiny striped jumping spiders, I apologize for failing to introduce you more fully to my species. And to the little male himself, I apologize for taking you from your habitat for no good reason.

Tropical field work in a metropolis

When I’ve told some friends I’m travelling to do field work in Singapore, they’ve said, “Huh?”. They pictured Singapore as a densely populated modern international metropolis, a 21st century human hive of tall buildings and precision infrastructure. I turns out, though, that Singapore has a good system of parks and reserves holding natural spider habitat of various kinds: tropical forest, swamp forest, mangrove, beach-side woodland. For a place so full of humans, it’s rather remarkable what Singapore has managed to preserve.

I have two scientific motivations to come to Singapore, and they are represented by the two arachnologists in Singapore with whom I’m working: Joseph Koh and Daiqin Li. I’ll explain my connections to both in separate blog posts, starting here, as did my visit, with Joseph.

Joseph Koh’s career has been to serve in government and NGOs by offering expertise and leadership, but I know him as a biologist, one of the world’s experts on southeast Asian spiders. He has worked for years to document and photograph the spiders of Singapore. You might think that all the spiders of Singapore would already be known, but just a taxi ride away from the hawkers’ markets there are several, probably many, species of jumping spider new to science. I’m here to help join Joseph reveal the jumping spider diversity of Singapore.

In the few days I’ve been in Singapore, Joseph and I have had a wonderful time talking spiders, along with his young assistant Paul Ng. We visited both nature reserves (Bukit Timah) and bits of urban nature. Joseph was wonderfully generous of his time and facilities (including his research lab and collection). After a few days, Joseph needed to leave to travel to a conference. Here is our farewell photo:

Myself (left) and Joseph Koh (right)

My student Kiran Marathe has since joined me for two more days of sampling. The initial explorations with Joseph, Paul and Kiran did indeed increase our knowledge of Singapore’s biodiversity, as we found the first females of Mintonia protuberans, and at least three undescribed species. We also learned more about the habitats of some classic southeast Asian jumping spiders, including these here:

Some familiar southeast Asian jumping spiders we’ve found so far in our visit to Singapore. The arrow by Thorelliola’s face shows the spike sticking forward like a unicorn’s horn on the face of the male.

A great start from a spider perspective, but also heartening with respect to conservation. I learned of Joseph’s decades-long efforts to build a relationship between Singaporeans and nature. Such a relationship was visible in the beautiful Bukit Timah Nature Reserve. On a holiday, we saw hundreds of people walking and running up the steep but well maintained trails, enjoying nature while getting exercise. You might think such a mass of people endangers the well-preserved forest, but the visitors take great care not to go off trail. In fact, we biologists felt like we were the transgressors, going off trail, as we needed to for our work. We much appreciated the respect shown to nature by those passing by as we poked about in the forest.

Please, don’t use CO1 barcodes alone for spider phylogeny

We systematists seeking to understand phylogenetic relationships of spiders need all the data we can get, and as easily as possible. There are few of us doing this work, and we have so many species to consider, that we could use a lot of help. It’s therefore tempting to look at the growing hoard of data from CO1 barcoding as a ready solution. But don’t, please don’t, use CO1 alone to reconstruct spider phylogenetic relationships.

CO1 (“cytochrome oxidase one”) is a mitochondrial gene that was chosen as the standard gene in animals to provide a natural “barcode” for identifying species. I won’t comment on how well it fulfills that task, except to say that I think it provides useful data, and that sometimes it works to distinguish species, sometimes it doesn’t. I will comment instead on how well it can be adapted to a different task: figuring out how species are genealogically related, looking back in time along the evolutionary tree. In the jumping spiders I have studied, CO1 is frequently highly misleading.

I’m provoked to say this because CO1 came into my consciousness, coincidentally, from four different directions this last week. Two colleagues independently mentioned they are planning or had planned to focus on CO1 for spider phylogenetics projects. I learned of a published paper that uses database-mined CO1 data, alone, to reconstruct phylogeny of some spiders. Finally, I was pulling together a phylogenetic analysis and looked to Genbank for additional data — where I found many sequences of CO1 from barcoding efforts. I will use those, but only because I have enough other data (both other genes and morphology) to overwhelm CO1’s flaws and provide the primary signal of evolutionary history.

What’s the problem with CO1? It frequently yields phylogenetic trees that are so bonkers, crazy, goofy that it can’t be trusted to stand on its own. How do I know that? By comparison with all other genes and morphology. Other genes we’ve studied well, 16SND1 (also mitochondrial!), 28S, Actin 5C, and wingless, produce phylogenetic trees on their own that largely make sense morphologically and that largely agree with one another.

CO1, on the other hand, is psychedelic. You can see that in Fig. 26 of Maddison et al. 2014 (ZooKeys 440: 57–87) shown below: the scattered pale blue lineages are all euophryines, clearly, by morphology and all other genes. Yes, there are moments of sanity (the purple hasariines hold together), but then CO1 simply loses it. You might rightly criticize this as a very sparse taxon sample for such a big group (shown in that figure is the major clade of >5000 species), but we’ve seen it in denser samples, the other genes do not suffer so, and the clade is probably rather young (<50 million years). We cite previous results from 2003 and 2012 showing that “CO1 struggles through both shallow and deep levels”. With a much denser taxon sample in the tribe Euophryini, Junxia Zhang and I (2013, Molec. Phyl. & Evol. 68: 81–92) found the CO1 tree to have regions of sanity but then some wildly broken parts, not only with members of other tribes and subfamilies jumping scattered into the midst of euophryines (Plexippus, Aelurillus, Heliophanus, Neon, Philaeus, spartaeines), but with members of a single genus (clearly, by all other data and geography) split far apart in the tree (Popcornella, Thyenula).

Salticinae portion of tree from CO1 (from Maddison et al. 2014)

I could focus my criticism on the sole use of a single gene, being way behind the times that we are now in, with phylogenomics giving us 500-gene results. Yes, we should have more data than just from a single gene, but it’s a matter of acceptable errors. With CO1, all signs are that its errors go beyond acceptable. CO1 is peculiarly misleading. Its mitochondrial colleague 16SND1 is not so bad, and while I’d still hesitate to base conclusions solely on it, from my experience it would make only small mistakes, not huge ones. And, as difficult as it may be to interpret, morphology alone is more reliable than CO1, as its basis is distributed throughout the genome. If one has only a single gene, morphological support for the results should be sought to improve their credibility. If that gene is CO1, I’d want to see a lot of morphological support.

Oh, had the barcoders only chosen a different gene!


Edits: hordes to hoard; through to throughout.