How did pygmy perch swim across the desert?

“Pygmy perch swam across the desert”

As regular readers of The G-CAT are likely aware, my first ever scientific paper was published this week. The paper is largely the results of my Honours research (with some extra analysis tacked on) on the phylogenomics (the same as phylogenetics, but with genomic data) and biogeographic history of a group of small, endemic freshwater fishes known as the pygmy perch. There are a number of different messages in the paper related to biogeography, taxonomy and conservation, and I am really quite proud of the work.

Southern_pygmy_perch 1 MHammer
A male southern pygmy perch, which usually measures 6-8 cm long.

To my honest surprise, the paper has received a decent amount of media attention following its release. Nearly all of these have focused on the biogeographic results and interpretations of the paper, which is arguably the largest component of the paper. In these media releases, the articles are often opened with “…despite the odds, new research has shown how a tiny fish managed to find its way across the arid Australian continent – more than once.” So how did they manage it? These are tiny fish, and there’s a very large desert area right in the middle of Australia, so how did they make it all the way across? And more than once?!

 The Great (southern) Southern Land

To understand the results, we first have to take a look at the context for the research question. There are seven officially named species of pygmy perches (‘named’ is an important characteristic here…but we’ll go into the details of that in another post), which are found in the temperate parts of Australia. Of these, three are found with southwest Western Australia, in Australia’s only globally recognised biodiversity hotspot, and the remaining four are found throughout eastern Australia (ranging from eastern South Australia to Tasmania and up to lower Queensland). These two regions are separated by arid desert regions, including the large expanse of the Nullarbor Plain.

Pygmyperch_distributionmap
The distributions of pygmy perch species across Australia. The dots and labels refer to different sampling sites used in the study. A: the distribution of western pygmy perches, and essentially the extent of the southwest WA biodiversity hotspot region. B: the distribution of eastern pygmy perches, excluding N. oxleyana which occurs in upper NSW/lower QLD (indicated in C). C: the distributions relative to the map of Australia. The black region in the middle indicates the Nullarbor Plain. 

 

The Nullarbor Plain is a remarkable place. It’s dead flat, has no trees, and most importantly for pygmy perches, it also has no standing water or rivers. The plain was formed from a large limestone block that was pushed up from beneath the Earth approximately 15 million years ago; with the progressive aridification of the continent, this region rapidly lost any standing water drainages that would have connected the east to the west. The remains of water systems from before (dubbed ‘paleodrainages’) can be seen below the surface.

Nullarbor Plain photo
See? Nothing here. Photo taken near Watson, South Australia. Credit: Benjamin Rimmer.

Biogeography of southern Australia

As one might expect, the formation of the Nullarbor Plain was a huge barrier for many species, especially those that depend on regular accessible water for survival. In many species of both plants and animals, we see in their phylogenetic history a clear separation of eastern and western groups around this time; once widely distributed species become fragmented by the plain and diverged from one another. We would most certainly expect this to be true of pygmy perch.

But our questions focus on what happened before the Nullarbor Plain arrived in the picture. More than 15 million years ago, southern Australia was a massively different place. The climate was much colder and wetter, even in central Australia, and we even have records of tropical rainforest habitats spreading all the way down to Victoria. Water-dependent animals would have been able to cross the southern part of the continent relatively freely.

Biogeography of the enigmatic pygmy perches

This is where the real difference between everything else and pygmy perch happens. For most species, we see only one east and west split in their phylogenetic tree, associated with the Nullarbor Plain; before that, their ancestors were likely distributed across the entire southern continent and were one continuous unit.

Not for pygmy perch, though. Our phylogenetic patterns show that there were multiple splits between eastern and western ancestral pygmy perch. We can see this visually within the phylogenetic tree; some western species of pygmy perches are more closely related, from an evolutionary perspective, to eastern species of pygmy perches than they are to other western species. This could imply a couple different things; either some species came about by migration from east to west (or vice versa), and that this happened at least twice, or that two different ancestral pygmy perches were distributed across all of southern Australia and each split east-west at some point in time. These two hypotheses are called “multiple invasion” and “geographic paralogy”, respectively.

MCC_geographylabelled
The phylogeny of pygmy perches produced by this study, containing 45 different individuals across all species of pygmy perch. Species are labelled in the tree in brackets, and their geographic location (east or west) is denoted by the colour on the right. This tree clearly shows more than one E/W separation, as not all eastern species are within the same clade. For example, despite being an eastern species, N. variegata is more closely related to Nth. balstoni or N. vittata than to the other eastern species (N. australisN. obscuraN. oxleyana and N. ‘flindersi’.

So, which is it? We delved deeper into this using a type of analysis called ‘ancestral clade reconstruction’. This tries to guess the likely distributions of species ancestors using different models and statistical analysis. Our results found that the earliest east-west split was due to the fragmentation of a widespread ancestor ~20 million years ago, and a migration event facilitated by changing waterways from the Nullarbor Plain pushing some eastern pygmy perches to the west to form the second group of western species. We argue for more than one migration across Australia since the initial ancestor of pygmy perches must have expanded from some point (either east or west) to encompass the entirety of southern Australia.

BGB_figure
The ancestral area reconstruction of pygmy perches, estimated using the R package BioGeoBEARS. The different pie charts denote the relative probability of the possible distributions for the species or ancestor at that particular time; colours denote exactly where the distribution is (following the legend). As you can see, the oldest E/W split at 21 million years ago likely resulted from a single widespread ancestor, with it’s range split into an east and west group. The second E/W event, at 15 million years ago, most likely reflects a migration from east to west, resulting in the formation of the N. vittata species group. This coincides with the Nullarbor Plain, so it’s likely that changes in waterway patterns allowed some eastern pygmy perch to move westward as the area became more arid.

So why do we see this for pygmy perch and no other species? Well, that’s the real mystery; out of all of the aquatic species found in southeast and southwest Australia, pygmy perch are one of the worst at migrating. They’re very picky about habitat, small, and don’t often migrate far unless pushed (by, say, a flood). It is possible that unrecorded extinct species of pygmy perch might help to clarify this a little, but the chances of finding a preserved fish fossil (let alone for a fish less than 8cm in size!) is extremely unlikely. We can really only theorise about how they managed to migrate.

Pygmy perch biogeo history
A diagram of the distribution of pygmy perch species over time, as suggested by the ancestral area reconstruction. A: the initial ancestor of pygmy perches was likely found throughout southern Australia. B: an unknown event splits the ancestor into an eastern and western group; the sole extant species of the W group is Nth. balstoniC: the ancestor of the eastern pygmy perches spreads towards the west, entering part of the pre-Nullarbor region. D: due to changes in the hydrology of the area, some eastern pygmy perches (the maroon colour in C) are pushed towards the west; these form N. vittata species and N. pygmaea. The Nullarbor Plain forms and effectively cuts off the two groups from one another, isolating them.

What does this mean for pygmy perches?

Nearly all species of pygmy perch are threatened or worse in the conservation legislation; there have been many conservation efforts to try and save the worst-off species from extinction. Pygmy perches provide a unique insight to the history of the Australian climate and may be a key in unlocking some of the mysteries of what our land was like so long ago. Every species is important for conservation and even those small, hard-to-notice creatures that we might forget about play a role in our environmental history.

Not that kind of native-ity: endemism and invasion of Australia

The endemics of Australia

Australia is world-renowned for the abundant and bizarre species that inhabit this wonderful island continent. We have one of the highest numbers of unique species in the entire world (in the top few!): this is measured by what we call ‘endemism’. A species is considered endemic to a particular place or region if that it is the only place it occurs: it’s completely unique to that environment. In Australia, a whopping 87% of our mammals, 45% of our birds, 93% of our reptiles, 94% of our amphibians 24% of our fishes and 86% of our plants are endemic, making us a real biodiversity paradise! Some lists even label us as a ‘megadiverse country’, which sounds pretty awesome on paper. And although we traditionally haven’t been very good at looking after it, our array of species is a matter of some pride to Aussies.

Endemism map
A map representing the relative proportion of endemic species in Australia, generated through the Atlas of Living Australia. The colours range from no (white; 0% endemics) or little (blue) to high levels of endemism (red; 100% of species are endemic). As you can see, some biogeographic hotspots are clearly indicated (southwest WA, the east coast, the Kimberley ranges).

But the real question is: why are there so many endemics in Australia? What is so special about our country that lends to our unique flora and fauna? Although we naturally associate tropical regions with lush, vibrant and diverse life, most of Australia is complete desert. That said, most of our species are concentrated in the tropical regions of the country, particularly in the upper east coast and far north (the ‘Top End’).

There are a number of different factors which contribute to the high species diversity of Australia. Most notably is how isolated we are as a continent: Australia has been separated from most of the rest of the world for millions of years. In this time, the climate has varied dramatically as the island shifted northward, creating a variety of changing environments and unique ecological niches for species to specialise into. We refer to these species groups as ‘Gondwana relicts’, since their last ancestor with the rest of the world would have been distributed across the supercontinent Gondwana over 100 million years ago. These include marsupials, many birds groups (including ratites and megapodes), many fish groups and a plethora of others. A Gondwanan origin explains why they are only found within Australia, southern Africa and South America (the closest landmass that was also historically connected to Gondwana).

Early arrivals and naturalisation to the Australian ecosystem 

But not all of Australia’s species are so ancient and ingrained in the landscape. As Australia drifted northward and eventually collided with the Sunda plate (forming the mountain ranges across southeast Asia), many new species and groups managed to disperse into Australia. This includes the first indigenous people to colonise Australia, widely regarded as one of the oldest human civilisations and estimated to have arrived down under over 65 thousand years ago.

Eventually, this connection also brought with them one of our most iconic species; the dingo. Estimates of their arrival dates the migration at around 6 thousand years ago. As Australia’s only ‘native’ dog, there has been much debate about its status as an Australian icon. To call the dingo ‘native’ implies it’s always been there: but 6 thousand years is more than enough time to become ingrained within the ecosystem in a stable fashion. So, to balance the debate (and prevent the dingo from being labelled as an ‘invasive pest’ unfairly), we often refer to them as ‘naturalised’. This term helps us to disentangle modern-day pests, many of which our immensely destructive to the natural environment, from other species that have naturally migrated and integrated many years ago.

Patriotic dingo
Although it may not be a “true native”, the dingo will forever be a badge of our native species pride.

Invaders of the Australian continent

Of course, we can never ignore the direct impacts of humans on the ecosystem. Particularly with European settlement, another plethora of animals were introduced for the first time into Australia; these were predominantly livestock animals or hunting-related species (both as predators and prey). This includes the cane toad, widely regarded as one of the biggest errors in pest control on the planet.

When European settlers in the 1930s attempted to grow sugar cane in the far eastern part of the country, they found their crops decimated by a local beetle. In an effort to eradicate them, they brought over a species of cane toad, with the idea that they would control the beetle population and all would be well. Only, cane toads are particularly lazy and instead of targeting the cane beetles, they just thrived on all the other native invertebrates around. They’re also very resilient and adaptable (and highly toxic), so their numbers exploded and they’ve since spread across a large swathe of the country. Their toxic skin makes them fatal food objects for many native predators and they strongly compete against other similar native animals (such as our own amphibians). The cane toad introduction of 1935 is the poster child of how bad failed pest control can be.

DSC_0867_small
This guy here, he’s a bastard. Spotted in my parent’s backyard in Ipswich, QLD. Source: me, with spite.

But is native always better?

History tells a very stark tale about the poor native animals and the ravenous, rampaging pest species. Because of this, it is a widely adopted philosophical viewpoint that ‘native is always best’. And while I don’t disagree with the sentiment (of course we need to preserve our native wildlife, and not the massively overabundant pests), there are rare examples where nature is a little more complicated. In Australia, this is exemplified in the noisy miner.

The noisy miner is a small bird which, much like its name implies, is incredibly noisy and aggressive. It’s highly abundant, found predominantly throughout urban and suburban areas, and seems to dominate the habitat. It does this by bullying out other bird species from nesting grounds, creating a monopoly on the resource to the exclusion of many other species (even larger ones such as crows and magpies). Despite being native, it seems to have thrived on human alteration of the landscape and is a serious threat to the survival and longevity of many other species. If we thought of it solely under the ‘nature is best’ paradigm, we would dismiss the noisy miner as ‘doing what it should be.’ The truth is really more of a philosophical debate: is it natural to let the noisy miner outcompete many other natives, possibly resulting in their extinction? Or is it only because of human interference (and thus is our responsibility to fix) that the noisy miner is doing so well in the first place? It’s not a simple question to answer, although the latter seems to be incredibly important.

Noisy miner harassing currawong
An example of the aggressive behaviour of the noisy miner (top), swooping down on a pied currawong (bottom). Despite the size differences, noisy miners will frequently attempt to harass and scare off other larger birds. Image source: Bird Ecology Study Group website.

The amazing biodiversity of Australia is a badge of honour we should wear with patriotic pride. Conservation efforts of our endemic fauna are severely limited by a lack of funding and resources, and despite a general acceptance of the importance of diverse ecosystems we remain relatively ineffective at preserving it. Understanding and connecting with our native wildlife, whilst finding methods to control invasive species, is key to conserving our wonderful ecosystems.

What’s the story with these little fish?

The pygmy perches

I’ve mentioned a few times in the past that my own research centres around a particular group of fish: the pygmy perches. When I tell people about them, sometimes I get the question “why do you want to study them?” And to be fair, it’s a good question: there must be something inherently interesting about them to be worth researching. And there is plenty.

Pygmy perches are a group of very small (usually 4-6cm) freshwater fish native to temperate Australia: they’re found throughout the southwest corner of WA and the southeast of Australia, stretching from the mouth of the Murray River in SA up to lower Queensland (predominantly throughout the Murray-Darling Basin) and even in northern Tasmania. There’s a massive space in the middle where they aren’t found: this is the Nullarbor Plain, and is a significant barrier for nearly all freshwater species (since it holds practically no water).

Unmack_distributions
The distributions of different pygmy perch species (excluding Bostockia porosa, which is a related but different group), taken from Unmack et al. (2011). The black region in the bottom right part indicates the Nullarbor Plain, which separates eastern and western species.

The group consists of 2 genera (Nannoperca and Nannatherina) and 7 currently described species, although there could be as many as 10 actual species (see ‘cryptic species’: I’ll elaborate on this more in future posts…). They’re very picky about their habitat, preferring to stay within low flow waterbodies with high vegetation cover, such as floodplains and lowland creeks. Most species have a lifespan of a couple years, with different breeding times depending on the species.

Why study pygmy perches?

So, they’re pretty cute little fish. But unfortunately, that’s not usually enough justification to study a particular organism. So, why does the Molecular Ecology Lab choose to use pygmy perch as one (of several) focal groups? Well, there’s a number of different reasons.

The main factors that contribute to their research interest are their other characteristics: because they’re so small and habitat specialists, they often form small, isolated populations that are naturally separated by higher flow rivers and environmental barriers. They also appear to have naturally very low genetic diversity: ordinarily, we’d expect that they wouldn’t be great at adapting and surviving over a long time. Yet, they’ve been here for a long time: so how do they do it? That’s the origin of many of the research questions for pygmy perches.

Adaptive evolution despite low genetic variation

One of the fundamental aspects of the genetic basis of evolution is the connection between genetic diversity and ‘adaptability’: we expect that populations or species with more genetic diversity are much more likely to be able to evolve and adapt to new selective pressures than those without it. Pygmy perches clearly contradict this at least a little bit, and so much of the research in the lab is about understanding exactly what factors and mechanisms contribute to the ability of pygmy perches to apparently adapt and survive what is traditionally not consider a very tolerant place to live. Recent research suggests the different expression of genes may be an important mechanism of adaptation for pygmy perch.

Recommended readings: Brauer et al. (2016); Brauer et al. (2017).

The influence of the historic environment on evolution

From an evolutionary standpoint, pygmy perches are unique in more ways than just their genetic diversity. They’re relatively ancient, with the origin of the group estimated at around 40 million years ago. Since then, they’ve diversified into a number of different species and have spread all over the southern half of the Australian continent, demonstrating multiple movements across Australia in that time. This pattern is unusual for freshwater organisms, and this combined with their ancient nature makes them ideal candidates for studying the influence of historic environment, climate and geology on the evolution and speciation of freshwater animals in Australia. And that’s the focus of my PhD (although not exclusively; plenty of other projects have explored questions in this area).

Bass Strait timelapse
The changing sea levels across the Bass Strait from A) 25 thousand years ago, B) 17.5 thousand years ago, and C) 14 thousand years ago (similar to today), from Lambeck and Chappel (2001). This is an example of one kind of environmental change that would likely have influenced the evolutionary patterns of pygmy perch, separating the populations from northern Tasmania and Victoria.

Recommended readings: Unmack et al. (2013); Unmack et al. (2011).

Conservation management and ecological role

Of course, it’s all well and good to study the natural, evolutionary history of an organism as if it hasn’t had any other influences. But we all know how dramatic the impact humans have on the environment are and unfortunately for many pygmy perch species this means that they are threatened or endangered and at risk of extinction. Their biggest threats are introduced predators (such as the redfin perch and European carp), alteration of waterways (predominantly for agriculture) and of course, climate change. For some populations, local extinction has already happened: some populations of the Yarra pygmy perch (N. obscura) are now completely gone from the wild. Many of these declines occurred during the Millennium Drought, where the aforementioned factors were exacerbated by extremely low water availability and consistently high temperatures. So naturally, a significant proportion of the work on pygmy perches is focused on their conservation, and trying to boost and recover declining populations.

This includes the formation of genetics-based breeding programs for two species, the southern pygmy perch and Yarra pygmy perch. A number of different organisations are involved in this ongoing process, including a couple of schools! These programs are informed by our other studies of pygmy perch evolution and adaptive potential and hopefully combined we can save these species from becoming totally extinct.

Yarra-breeders-vid.gif
Some of the Yarra pygmy perch from the extinct Murray-Darling Basin population, ready to make breeding groups!
Fin clipping Yarras.jpg
Me, fin clipping the Yarra pygmy perch in the breeding groups for later genetic analyses. Yes, I know, I needed a haircut.

Recommended readings: Brauer et al. (2013); Attard et al. (2016); Hammer et al. (2013).

Hopefully, some of this convinces you that pygmy perch are actually rather interesting creatures (I certainly think so!). Pygmy perch research can offer a unique insight into evolutionary history, historical biogeography, and conservation management. Also, they’re kinda cute….so that’s gotta count for something, right? If you wanted to find out more about pygmy perch research, and get updates on our findings, be sure to check out the Molecular Ecology Lab Facebook page or our website!