Sunday, March 23, 2014

Darwin’s Pub

Surely the greatest contribution that England has made to the world (apart from deep-fried Mars bars) is Charles Darwin. Certainly, then, the most important tourist destinations in England should be sites associated with Darwin. At least, that has always been my opinion. This post is about my failures and successes in attempting to visit Darwin’s haunts – and a few unexpected and uncommon discoveries along the way.

Would Chuck D have partaken?
On my first visit to London a number of years ago, I had half a day to spare and so sought out Darwin’s grave at Westminster Abbey. I showed up at the door, all aquiver with anticipation, only to be told that it was the one day of the year when tourists were not allowed – a special day instead for worship only. Damn. The next time I visited England, I had a whole day to spare (owing to that annoying policy of airlines charging almost double if you don’t stay over a Saturday night) and so I set my sights on a pilgrimage to Darwin’s home, Down House. Seeing his study and walking his Sandwalk, his “thinking path,” would surely be a great inspiration – and it must certainly be on the bucket list of every evolutionary biologist. After arriving in London on that trip, I looked Down House up on the internet and discovered that it was closed for renovations. Double damn. Instead, I visited the British Natural History Museum, where I could at least see the statue of Darwin. This statue figured prominently in a David Attenborough video for Darwin’s 200th birthday that explained how the statue of Richard Owen, who was instrumental in the museum’s history but a vocal critic of evolution, had recently been removed and replaced by this monument to his archrival Darwin.

Westminster Abbey
I visited London again last week, and I promised myself that I would visit both Darwin’s grave and his home. I even checked the opening times of Down House before booking my flight – Saturdays and Sundays only. So, on the Friday after our bioGENESIS meeting (see this post), I set out for Westminster Abbey. After waiting in line for nearly an hour, I finally made it inside. It was crowded and I was awash in hundreds of graves and monuments all over the floor and walls. Where was Darwin? The audio guide didn’t mention him – as I had been certain it would – so I had to ask. It turned out to be a plain white marble slab on the ground. I had expected something more dramatic, maybe with finch beaks engraved on it, but it was still fun to see the grave and compose pictures of it with the backdrop of an institution that – initially at least – felt so threatened by his ideas. After leaving Darwin’s grave, I tried to take a photo of the “grave of the unknown soldier” (definitely on the audio guide) and was promptly informed that photos were not allowed in the Abbey. Oops. I guess no one cares enough about Darwin’s grave to guard against photography. Even so, it was great to see the founder of evolutionary biology buried in the most important religious institution in England. (Writing this, I wonder if Bishop “Soapy Sam” Wilberforce is also in the church, perhaps with a perpetual frown in Darwin’s direction. Or maybe he is in some lesser church, with an even bigger frown.)

Westminster Abbey
The next day I was off for Down House, which proved to be quite a commute from the hotel, as befit Darwin’s desire to escape the city. I was even forced to wait about an hour for the bus from South Bromley to Downe Village (the “e” was added after Darwin’s time to distinguish it from another Down elsewhere). Fortunately, a Starbuck’s was right beside the bus stop, and so I could sip a non-fat no-whip hot chocolate (tastes the same the world over) and edit a paper. Eventually the bus came and about 20 minutes later we stopped at St. Mary’s Church in Downe. From there it was a 10 minute walk along a narrow lane between some fields and I had the great fun of seeing a pheasant prancing about – did Darwin shoot at its ancestors and miss? Down House was amazing, of course, particularly Darwin’s study and his thinking path, where I made a video to ask the pressing question: How did Darwin walk his sandwalk?

I could well have written an entire post about the wonders of Down House: Darwin loved billiards and would play every day with his butler, Darwin would leave his office dozens of times a day just to get a pinch of snuff from the hallway outside, Darwin rode horses until he fell and gave up, and so on. However, what happened after I left proved to be even more surprising and inspiring and so I will turn to that story.

Submitting a paper at Down House.
After about four hours at Down House, I walked back to the church in Downe to catch the bus. I had a few minutes to spare and so I walked around the church (and saw a plaque saying the sundial was in Darwin’s honor) and in the church (where written material explained how Darwin and his butler, Mr. Parslow, were an integral part of the community). As the bus was arriving, I saw a pub across the street from the church – the George & Dragon. Hmmm, I thought, how could I not have a drink in the bar in Darwin’s home town? So I let the bus go by, committing myself to at least an hour in Downe, and walked across the street to have a pint of Guinness. On my way there, I started to wonder. Could Darwin have gone to this pub? It looked quite old – perhaps he stopped in for a beer or two. Or maybe he spent the whole church service there after his beloved daughter Annie died and his faith was thus permanently shattered.

Emma’s church.
I entered the pub and was reinforced in my romantic hope as it looked really old, down to the low ceiling with rough-hewn and sagging support beams. But it still seemed a silly hope, so I started by asking the bartender some leading questions. “How old is Guinness?” – “Oh, hundreds of years.”  “Cool – and how old is this pub.” – “Oh, considerably older than Guinness.”  “Really,” I say, my excitement mounting. “Could Darwin have come in here for a pint.” – “Oh, yes, certainly. In fact, he stayed upstairs while visiting Downe and looking at the house.”  “Awesome. Perhaps he had a pint of Guinness here – just like I am doing.” – “Oh, that seems likely as he did some business here – see the photo and inscription on the wall.”

Darwin’s pub – the George and Dragon
Guinness in hand, I walk over to a framed document, which included a picture of the pub in the old days – originally called the George Inn – accompanied by an excerpt from the Bromley Record, July 1, 1867.

On Tuesday, 11th June, the Downe Friendly Benefit Society held their 17th anniversary at the GEORGE INN where a most excellent dinner was provided by Mr. and Mrs. Uzzell. The chair was taken by Mr. Snow and the vice-chair by Mr. Parslow. After the cloth was removed and the usual loyal toasts and healths of the treasurer C. R. Darwin Esquire and others, had been given …

Be still my beating heart.

Over the next few hours, I sat in a big comfy chair beside a fireplace that might have warmed Darwin (but not me, owing to fire regulations) and drank several pints while bus after bus went by without me. I edited a paper about the evolution of resistance to parasites. I edited the video asking How did Darwin walk his sandwalk? And I generally absorbed the ambiance and reveled in the thought that I might be sitting in the place where Darwin first scribbled his “I think” diagram – perhaps on a bar napkin.

Darwin’s thinking chair?
OK, I realize I am being overly romantic here. Guinness was probably not on tap in 1860. And, if it was, it was probably not available in the George Inn. And, if it was, Darwin’s delicate stomach probably made him gravitate toward easier fare. And bar napkins probably didn’t exist. And, if they did, Darwin probably didn’t bring his quill to the bar. And, if he did, he probably wasn’t thinking about evolution while drinking. And, of course, he probably scribbled his I think diagram somewhere else (indeed, he did so before buying Down House). But the experience was nevertheless inspiring and the scenario at least plausible in that Darwin might have had some eureka moments in the same physical location I was occupying. Certainly, most of my good ideas have come in bars over a pint of beer or a glass of whisky – at least most of my good blog ideas anyway.

Or maybe Darwin would have preferred this sherry - photo by Mike Hendry
So, the next time you’re in England, by all means visit Darwin’s grave and Down House. Marvel at his writing chair. Be inspired on the sandwalk. But – most of all – don’t forget to visit Darwin’s pub. Bring your computer – do some science. Darwin would want you to.

Wednesday, March 19, 2014

From a conundrum to the mosaic of reproductive isolation

[ This post is by Katja Räsänen; I am just putting it up.  –B. ]

In a paper published in a special issue on ecological speciation in 2012 (Räsänen et al. 2012, J. Int. Ecol), we showed that lake and stream threespine stickleback (Gasterosteus aculeatus) from the Misty system, Vancouver island, Canada, do not mate assortatively by ecotype. This apparent lack of mating barriers between highly distinct ecotypes contrasts strongly with the findings from the benthic-limnetic stickleback (now a central model for ecological speciation) and posed us with an intriguing conundrum.

For all of you who struggle with the word “conundrum”: according to Wikipedia it is “a riddle whose answer is or involves a pun or unexpected twist” and/or “a logical postulation that evades resolution, an intricate and difficult problem”. The lake and (inlet) stream fish from the Misty system are phenotypically very divergent (even when reared in the lab over multiple generations) and genetically distinct, yet there are no strong geographic barriers to movement between the lake and its inlet or outlet streams. To us this indeed is a riddle – but does the answer involve a pun or an unexpected twist? That is yet to be seen. It certainly is logical to postulate that we would expect there to be some form of strong reproductive barrier between clearly genetically distinct populations – when there are no strong barriers to movement of individuals. So, if assortative mate choice (e.g. via the “mate with your own type” rule) is not the reproductive barrier, what then keeps these ecotypes distinct?

Reproductive isolation (RI) can arise via many different ecologically and non-ecologically mediated pre- and post-mating barriers. (See Nosil et al. 2005, Evolution 59: 705-719 for a nice overview). For the Misty stickleback, we have evidence that assortative mate choice is weak or non-existent and that genetic incompatibilities are unlikely (hybrid crosses are easy to perform and hybrids are viable). So in a recently published paper (Räsänen and Hendry 2014, Ecology and Evolution), we report on the next step in our hunt for reproductive barriers in this system. Here we tested for selection against migrants (SAM), whereby individuals from populations adapted to a given environment (for example, a lake) are selected against when migrating to other environments (for example, a stream).

What makes the Misty system particularly interesting in this context is that two streams are connected to the lake: the inlet stream, where water flows into the lake, and the outlet stream, where water flows out of the lake. (Why the direction of flow matters, I will return to below). Previous work has repeatedly demonstrated that Inlet stickleback are phenotypically and genetically strongly divergent from the Lake fish, whereas Outlet stickleback are phenotypically and genetically pretty similar to the Lake fish (especially close to the lake).

IMAGE 1.  Representative individuals of wild caught threespine stickleback from the Misty system. Typically, Inlet fish are smaller, deeper bodied and more drab in colouration, whereas Lake and Outlet fish have shallower and more streamlined bodies and darker colouration. These differences are genetically based. © A.P. Hendry.

This difference in divergence has been suggested to reflect the balance between adaptive divergence and gene flow: gene flow from the lake to the outlet is higher at least in part due to the ease of dispersing in the direction of the water flow, combined with the large population size of lake stickleback, whereas gene flow from the lake to the inlet is apparently constrained at least in part because stickleback, unlike salmonids, do not like to swim upstream. However, if the strong phenotypic and genetic divergence between the Lake and Inlet stickleback does reflect adaptive divergence, we would expect any individuals moving to the “wrong” environment to be selected against due to their reduced performance: selection against migrants (SAM), as described earlier.

To test for SAM, we conducted a reciprocal transplant experiment in situ using enclosures. For this, we used fish that were collected from the wild – and hence express the full phenotype within a given environment (keeping in mind here that it is the composite phenotype, including direct genetic, epigenetic, parental and environmental effects, that is under selection in the wild). We erected enclosures in the lake, outlet, and inlet, and then transferred a randomly selected subset of mature-size fish from each site to each enclosure.

IMAGE 2. I am releasing fish to the Inlet enclosure.

We made sure the fish were in good shape prior to transfer, tagged them with coded wire tags, weighed them (to get a grasp of size differences) and photographed them, and then released the fish for three weeks to do whatever fish like to do in a lake or in a stream environment. (Presumably mostly eating the local food and “socializing” – positively or negatively – with their neighbours…)

We made two key predictions. First, since Lake and Inlet fish are strongly phenotypically different (Inlet fish are smaller, deeper bodied and have fewer and shorter gill rakers than Lake fish), whereas Lake and Outlet fish are phenotypically similar (pretty big buggers, with dark blue nuptial coloration, and more limnetic-type feeding morphology), we predicted that Lake and Inlet fish should perform differently, whereas Lake and Outlet fish should perform similarly in all environments. Second, if each population is locally adapted to its native environment, we would expect that each ecotype (Lake, Inlet or Outlet) should perform best in its native environment (Lake in lake, Inlet in inlet…and so on). (Of course, given that our Outlet fish are phenotypically similar to the Lake fish, they should perform well in the lake too…)

It is this second prediction that is the key prediction for SAM: if SAM contributes to RI, we would expect that Inlet fish perform poorly when transferred to the Lake (= Inlet fish would be selected against in the lake), whereas Lake fish perform poorly when transferred to the inlet (= Lake fish would be selected against in the inlet). Nice and easy!

But what did we find?

For the first prediction – yes indeed, phenotypically different Inlet fish did perform differently from Lake (and Outlet) fish in all environments, whereas the phenotypically similar Outlet and Lake fish performed similarly in all environments. (The measures of performance here being change in body mass and survival). This confirmed that phenotype does make a difference for fitness. All good. However, for the second prediction the results were not quite what we would have expected. Basically, although Inlet fish indeed did perform poorly in the lake (they lost a lot weight and had much lower survival), Lake fish seemed to be quite content in the inlet (they had high survival and did not lose much weight).  (For the result details, do check the paper…)

This finding suggests that SAM in the Misty system is asymmetric: it works in one direction (from the inlet to the lake), but not in the other (from lake to the inlet). (I now ignore the Outlet fish as they don’t do much that is unexpected). Ok…so what does this then mean for the conundrum? Does it help to solve the riddle?

Well, yes – partially. It does suggest that SAM indeed makes some contribution to RI – by reducing gene flow from the Inlet to the Lake population. But why do Lake genotypes then not swamp the Inlet?  This is particularly worth asking given that the Lake population (in addition to outperforming Inlet fish in the inlet) is very large and the Inlet population is rather small… so by sheer numbers you’d expect gene flow to constrain adaptive divergence also in the Inlet (unless migrants are selected against, that is). So why does this not happen? There could, of course, be many different reasons. Firstly, given that our experiment only ran for three weeks (and not the whole life-cycle), it may be that we just didn’t pick up the whole suite of performance differences. Secondly, as piscivorous fish and diving birds were not allowed access to the enclosures, most of the performance differences we saw were likely mediated via diet and social interactions (e.g. competitive aggression) and it may be that we excluded some important selective factors.

Or maybe it could be that other reproductive barriers are important? One possibility is temporal isolation (different breeding times). Another is habitat choice… and here we are back where I started: maybe Lake fish just don’t like to move upstream, and thus stay put in the lake (when not venturing to the outlet). This could very well be the case given that several studies by the Hendry and Bolnick labs suggest that sticklebacks don’t readily venture against the flow.

The key, however, is – and here I come back to the word “mosaic” in the title – that maybe, instead of looking for one magic trait and one major reproductive isolating barrier (typically mate choice or genetic incompatibilities), we should be thinking of reproductive isolation as a composite of several different reproductive barriers that can vary in strength and direction. They may be asymmetric (as SAM seems to be in our case), but together with other barriers (possibly habitat choice in our case) they could result in strong TOTAL isolation.

Evidence for such mosaic isolation is certainly emerging from some systems (such as Timema walking sticks, Ischnura damselflies or Mimulus monkeyflowers)… so maybe the solution to the conundrum rests in understanding the relative strength of a multitude of reproductive barriers. There is only one way to know how common single major barriers versus a mosaic of weaker barriers are in nature. So, if you didn’t find evidence for RI in your pet system based on some single mechanism, keep looking!

IMAGE 3. Our mission (at least partially) accomplished! Now it’s your turn... © A.P. Hendry.

Sunday, March 16, 2014

Extinctive – a new addition to the lexicon of biodiversity science?

Much debate in science revolves around terminology – indeed, whole papers are written about specific words. A personal favorite – if only for the title – is Ontoecogenophyloconstraints by Antonovics and van Tienderen. For some reason, terminological issues seem particularly acute in the context of biodiversity science. What precisely are “ecosystem services”? What is sustainability? Tipping points? Earth system services?

As a result, we sometimes get into terminological debates at our bioGENESIS meetings – a few years ago in Cape Town, we even coined a new term “evosystem services.” This term arose from the realization that all ecosystem services are the product of organisms, and all organisms are the product of evolution. One plus one must mean that all past, present, and future ecosystem services are also EVOsystem services. This recognition is important because it makes clear the need to inject evolutionary thinking into biodiversity science, a goal that is – after all – the raison d'etre of bioGENESIS. We (mainly Dan Faith) invented this term over dinner on the edge of the Southern Ocean in Cape Town, and I can remember drawing a circle labelled “ecosystem services” surrounded and completely enveloped by another circle labelled “evosystem services”. The point was that not only are all recognized ecosystem services also evosystem services, but evolution provides many services (past, present, and future) that are not encapsulated by the usual view of ecosystem services. (We had imbibed enough to later draw another even more inclusive circle – geosystem services – and around that another circle – cosmosystem services – and around that yet another circle – theosystem services.)

Spring has sprung at Kew.
This week I attended another bioGENESIS meeting, this time at the Kew Royal Botanical Gardens in London, England – graciously hosted by Felix Forrest. And – yet again – we debated terminology, including the very same words we had debated at past meetings. This time, however, we ended in a different place. We were having dinner at a nice French restaurant (perhaps the best way to be sure of good food in England), and we started considering the meaning of the term “distinct,” which led us to contrast it with “distinctive.” In an effort to figure out how these terms differed, we started considering other words ending in “tinct” to which one could also add “ive” on the end. Instinct versus instinctive, indistinct versus indistinctive, and extinct versus extinctive. Huh? Extinctive? Is that even a word? We had never heard it before and thus reasonably assumed it did not exist in the English language.

Spring has sprung at Kew.
What might “extinctive” mean – if it were to mean anything at all? We decided it would likely mean “having the properties of being extinct without actually being extinct” – at least not yet. The term might thus apply to species that were sure to go extinct in the reasonably near future: that is, a species experiencing an “extinction debt” or “extinction in waiting”. After all, this definition seemed to fit fairly well with “instinct” versus “instinctive.” As an example, Pinta Island giant tortoises were extinctive for 40 years, right up until Lonesome George died just a few years ago. We were having a good time with this debate (at least I was) until Felix got out his smart phone and started looking up words. It turns out that the above four words are the only ones in English to end in “tinct” and, of these, extinct is the only one to which one cannot add an “ive” on the end. Cool! Oops – not true. It seems that extinctive is actually a real word (“tending or serving to extinguish or make extinct”), which presumably preempts our new definition. (Hell, while writing this, I can see that MSWord’s spell checker doesn’t even flag it. If Bill Gates says it is a word, it must be. Then again, while posting it, I see that Blogger does flag it - so Google says it isn't a word. Clash of the Titans!)

Felix showing us what might well be the world's most biodiverse square meter - the genomic DNA storage facility at Kew.
So the great debate ended in a whimper … until Dan pointed out that instinguish was definitely not a word – but should be. And so it went …

Dan demonstrating how to instinguish.

Some earlier posts about evosystem services:

The bioGENESIS crew at Kew: Luc, Felix, Geeta, Lucia, Anne-Helene, Keight, Dan, Melina, and Andrew

Wednesday, March 12, 2014

Evolution in small spaces: microgeographic adaptation and the spatial scale of evolution

Local adaptation has been the focus of intense study for many decades. Given how widely it has been observed across diverse taxa and ecological settings, one may not be too far out on a limb in saying that it is the default evolutionary scenario when suitable conditions exist. But we rarely reflect on what is “local” about this adaptation. In fact, the “local” moniker can be rather misleading. Local adaptation occurs when a population evolves traits that result in higher fitness of native individuals in the home environment relative to individuals from foreign populations, regardless of spatial scale. In a review article in this month’s issue of Trends in Ecology & Evolution, Mark Urban, Dan Bolnick, Dave Skelly, and I lay out the arguments for why we need to think about space more explicitly in studies of local adaptation, particularly at fine spatial scales.   

For example, the classic common garden experiment by Clausen, Keck and Hiesey in the 1930s was a beautiful demonstration of local adaptation in Potentilla glandulosa, a small flowering herb that shows clear divergence in several traits along a ~300 km transect (and 3.6 km elevation gradient). This is an example of local adaptation at a large spatial scale and, more importantly, with the low gene flow expected between the populations investigated. In this sense, adaptive divergence in Potentilla will not surprise most evolutionary ecologists – populations experience very different environments and share little gene flow, allowing them to adapt to their local natural selection regimes without intrusion of maladaptive gene flow.

Clausen, Keck and Hiesey’s 300 km transect and morphology of Potentilla glandulosa populations used in their common garden experiment. Individuals were transplanted to three locations (Stanford, Mather and Timberline) where the experiments were done, demonstrating a genetic basis for local adaptation at a large spatial scale.
Compare that example with local adaptation happening at much finer spatial scales. Evolutionary divergence at very small scales has largely been discounted as unlikely, due primarily to expectations of high gene flow that is expected to disrupt any incipient divergence. Yet more and more examples of fine-scale local adaptation are being documented and reported every year. The threespine stickleback (Gasterosteus aculeatus) provides important examples of this fine-scale adaptation. Data from Andrew Hendry’s lab suggest that stickleback body morphology diverges dramatically between fish separated by tens of meters between lake and adjoining stream habitats (e.g., Hendry & Taylor 2004; Moore & Hendry 2005). At even finer scales, Dan Bolnick’s group has found divergence in stickleback size, coloration, trophic position and diet across only a 1–2 meter cline of water depth in these highly mobile fish (e.g., Snowberg & Bolnick 2012).

Left: A typical inlet stream entering a lake habitat on Vancouver Island in British Columbia. Phenotypic divergence has been documented at this small spatial scale between stickleback inhabiting the inlet (and outlet) streams and the pond basin. Right: Within a lake, stickleback males can evolve divergent coloration, size and trophic position along a water depth gradient of only 1–2 meters. Photos by Dan Bolnick and Chad Brock.
One of the aims of our TREE review article is to highlight the empirical support for and theory behind evolutionary divergence at small spatial scales. However, “small spatial scales” is entirely relative to the study species being investigated and their dispersal attributes. For this reason, we advance three main concepts in our review:

1. We propose a metric called the “wright” that measures phenotypic divergence across space while standardizing this divergence based on the dispersal of the organism. The “wright” is scaled to the dispersal neighborhood of a species or population, representing all of the individuals located within a radius extending two standard deviations from the mean of the dispersal distribution (i.e., dispersal kernel). Scaling the metric based on dispersal allows comparisons of the degree of adaptive divergence among species with very different dispersal abilities. For example, significant phenotypic divergence between two populations of songbirds situated 100 meters apart will be far more unexpected than divergence between snail populations over the same Euclidean distance. However, by scaling the divergence observed by the number of dispersal neighborhoods separating those 100 meters, we can compare the differentiation between birds and snails in a meaningful way. We coined the term “wright” for this metric because of Sewall Wright’s development of the dispersal neighborhood (also called the “gene flow neighborhood”, “Wright’s neighborhood” or “panmictic unit”), and the fact that it is a direct analog to the previously defined “haldane”, a measure of divergence through time.

2. We establish a threshold for distinguishing evolution at fine spatial scales, and formalize the definition of microgeographic adaptation. The microgeographic term has long been used, albeit inconsistently, to describe local adaptation at small spatial scales. This includes divergence across 25 meters in snails to 40 kilometers in brown trout. In order to be applied consistently across studies and species, we define microgeographic adaptation as adaptive divergence occurring within one dispersal neighborhood, an area where dispersal is expected to be frequent enough to prevent genetic drift. In this way, microgeographic adaptation is defined as a special case of local adaptation occurring at spatial scales where populations should experience high gene flow based on the expected levels of dispersal.

Top: A hypothetical landscape with three forest patches of the ‘light’ and ‘dark’ variety supporting populations of a moth species with two distinct color morphs. Each morph has higher fitness on the trees more closely matching their color and providing better camouflage. Bottom: The dispersal distribution (i.e., kernel) for this moth overlaid on the focal ‘light’ forest patch. The red circle delineates the dispersal neighborhood proposed by Wright, with a radius of two standard deviations from the mean of the kernel. Microgeographic adaptation occurs when two populations separated by less than one neighborhood radius adaptively diverge (e.g., the moth morphs diverge between the two forest patches under the kernel). Divergence between sites outside of this neighborhood would be considered local adaptation, but not microgeographic (e.g., between the light forest and the dark forest patch to the left). Adapted from Richardson et al. 2014.
3. We evaluate seven mechanisms that can either initiate or amplify adaptive divergence at fine spatial scales. Microgeographic adaptation is of particular interest because it occurs despite the high potential for mixing between nearby populations, making it unlikely that neutral processes can generate appreciable variation at this scale. This divergence requires some process that increases the strength of natural selection or reduces maladaptive gene flow relative to dispersal ability. The full list can be found in the paper; however, non-random gene flow (e.g. habitat choice and phenotypic sorting), spatially autocorrelated selection regimes, and selective barriers against migrants are three mechanisms that may commonly contribute to microgeographic adaptation.

We also highlight notable examples of microgeographic adaptation, consider broader implications of fine-scale adaptation for ecology and evolutionary biology, and conclude with a discussion of the immense opportunities that exist to more explicitly integrate spatial scale into evolutionary ecology. This includes specific recommendations for evaluating evolutionary processes at fine spatial scales.

The most salient messages we hope result from this article are that (1) we need to start considering space explicitly by incorporating spatial considerations into any study design, (2) understanding the role of dispersal and gene flow is critical to understanding the scale of evolution, and researchers should make a more concerted effort to characterize and quantify the dispersal distributions of our study species, (3) researchers should integrate observations of natural selection, standard experimental methods (e.g, common garden and transplant experiments) and innovative approaches (e.g., introduction and tracking of maladapted genotypes) with an eye towards understanding the minimum scale of evolutionary divergence and the mechanisms driving this divergence, and (4) a standard measure of evolution across space is needed to compare divergence across multiple species. Our hope is that the “wright” will catalyze the collection of data needed to evaluate the generality of microgeographic adapation in nature. Abundant opportunities also exist for creative manipulations of natural selection, dispersal and the genetic makeup of populations in the wild in order to understand how evolution operates at small scales.

After our review was in press, we had a chance to present these ideas as part of a symposium at the January meeting of the American Society of Naturalists at Asilomar in California. The response then and since the article was published has been exceedingly positive. The one objection that has come up several times is from researchers asserting that we have known about and appreciated fine-scale adaptation for a long time. With some probing, however, what they are generally referring to is divergence occurring at spatial scales that are “surprising” to the investigator in that system. Perhaps that’s a necessary starting point, but with this article and the standardized “wright” metric we are trying to move away from subjective assessments of what scales are surprising, to quantitative evaluations of the spatial scale of evolution.

The paper:

Richardson JL, Urban MC, Bolnick DI, Skelly DK. 2014. Microgeographic adaptation and the spatial scale of evolution. Trends in Ecology & Evolution 29 (3): 165-176.    

Friday, March 7, 2014

Anthropogenic habitat disturbance can impact species integrity

[ This post is by Dan Hasselman; I am just putting it up.  –B. ]

“Help… we need reinforcement!”

A major focus of my research deals with understanding how human activities impact the long-term persistence of species and influence evolutionary and ecological processes. Human activities are increasingly recognized as a potent evolutionary force shaping contemporary patterns and processes among populations, species, and ecosystems. From size-selective harvesting and over-exploitation to the myriad consequences of urbanization, the evolutionary and ecological impacts of humanity on natural systems are pervasive. Consider the consequences of anthropogenic alterations to a species’ habitat. Habitat modification can threaten the integrity of young evolutionary lineages by smoothing rugged adaptive landscapes that promote and maintain diversification in sympatry. The loss of environmental heterogeneity via human activities can relax disruptive selection and can lead to the breakdown of nascent (intrinsic and extrinsic) reproductive isolating mechanisms, facilitating introgressive hybridization and the collapse of incipient species into a hybrid swarm (i.e., “reverse speciation”). Although species with deeper evolutionary histories are not immune to the evolutionary consequences of anthropogenic habitat disturbance, the formation of a hybrid swarm between divergent species that naturally occur in sympatry is not well established. Indeed, under these conditions, evolutionary theory predicts that reinforcement (in the “broad sense”; sensu Servedio and Noor, 2003) should sustain reproductive isolation among divergent lineages in sympatry and confer some level of resistance to habitat disturbance. However, my research with the Palkovacs Lab (UC Santa Cruz) on anadromous (i.e., migratory sea-run) river herrings suggests that this is not always the case.

Our research group at UC Santa Cruz, along with our colleagues at Duke University and Dalhousie University, recently examined the range-wide incidence of hybridization and patterns of introgression between alewife (Alosa pseudoharengus) and blueback herring (A. aestivalis), species that diverged up to 1 million years ago. Although anadromous populations of these species co-occur in numerous rivers along the Atlantic coast of North America, reproductive isolation is typically maintained by differences in spawning time and spawning habitat preferences. While differences in peak spawning time are subtle (2–3 weeks) and lead to considerable temporal overlap in rivers, alewife preferentially select lentic (i.e., still-water) habitats for reproduction, whereas blueback herring prefer lotic (i.e., flowing-water) spawning habitats.  However, the construction of a dam on the Roanoke River, Virginia, in 1953 resulted in the formation of landlocked populations of both species. This created novel conditions for alewife and blueback herring in Kerr Reservoir, and provided our research team with an opportunity to examine the effects of habitat disturbance on the frequency of hybridization and patterns of introgression between divergent species that naturally occur in sympatry.

Fig. 1. Anthropogenic changes to habitat, like dams that block migratory anadromous fishes, have the potential to impact evolutionary and ecological processes.  Here, anadromous alewives school below a dam on the Damariscotta River, Maine (photo: Heather Perry).

Using 15 microsatellites, I conducted simulations and examined empirical data to identify anadromous and landlocked hybrids with two complimentary Bayesian analyses. I also conducted an analyses of genomic clines (Gompert and Buerkle 2009) to identify whether the pattern of introgression differed among anadromous and landlocked hybrids.

Although the proportion of hybrids among anadromous populations was generally low (0–8%), all of the individuals in Kerr Reservoir (n=119) were deeply introgressed hybrids, and comprised a hybrid swarm. These results suggest that the pre- and post-zygotic reproductive isolating mechanisms that facilitate the maintenance of species integrity for anadromous parental populations may have broken down in Kerr Reservoir, and that there may not be selection against hybrids in this altered environment. The precise mechanisms that lead to the persistence of landlocked river herring hybrids are not currently understood.

While anadromous hybrids were intermediate in their genetic composition between alewife and blueback herring, landlocked hybrids exhibited genetic compositions that were clearly different from either parental species (see Fig. 2, below). While this suggests evidence for genetic divergence of landlocked hybrids in isolation from parental species, it is uncertain whether this may provide evidence for hybrid speciation in the future. The genomic clines analyses revealed striking differences in the patterns of introgression, with anadromous hybrids exhibiting neutral patterns of introgression, and landlocked hybrids showing directional introgression leading to an increased prevalence of alewife genotypes in Kerr Reservoir.

Fig. 2. Factorial correspondence analysis revealed two factors that explained 85.6% of the genetic variation among purebred and hybrid river herring, and demonstrated the clear separation of landlocked hybrids in Kerr Reservoir from alewife, blueback herring and anadromous hybrids.

Our study reveals that anthropogenic habitat disturbance can break down reproductive isolation between divergent species that naturally occur in sympatry, and provides empirical evidence that reinforcement does not always sustain reproductive isolation under such circumstances. Dam construction constitutes a dramatic alteration to habitat, particularly for anadromous fishes, and may disrupt the processes that facilitate reproductive isolation and maintenance of species integrity. The removal of dams is often couched in terms of benefits to anadromous fishes and restoration of historic spawning runs. Our work suggests that dam removal can also help to maintain species integrity.

If you’d like to read about this study (Hasselman et al., 2014) in more detail, you can find it here:

– Dan Hasselman (

Tuesday, March 4, 2014

Basque fish now have a blog!

[ The author of this post is Jacques Labonne; I am just putting it up for him.  –B. ]

Once upon a time, in a far, far-away kingdom, an indomitable neolithic1 tribe resisted invaders as well as the king’s men for centuries, maybe for millenia. Gauls, Romans, Visigoths, Franks, and more recently the Spanish and French – this outlier of European culture resisted phagocytosis by all of them. Centuries passed, and because the evil French government could not tolerate such a provocation, and also because brute force and cultural propaganda dismally failed, a more subtle approach was attempted: remain firm and inflexible, but also, invest money and time in the development of the Basque Country. As a result, this tribe, known as the Basque, still thrives, culturally and genetically2.

The blessed Atlantic swell on the Basque coast.

That is how a small research station, mostly dedicated to the study of fish biology, aquaculture, and ecology, came into existence in the 70’s, wedged between the Atlantic Ocean and the Pyrénées mountains.

An aerial point of view on the Basque countryside and hills, with the lab and the facilities.

People now working in this facility, when they are not Basque themselves, tend to evolve the same traits as the local population: they get a bit isolated from the rest of the country, spend a lot of time partying, and either remain at the research station, or leave the country for remote intercontinental destinations. Bimodal dispersal kernel.

A handful of these people are investigating the behavioural ecology of fish, either in controlled lab experiments, in semi-natural environments, or in wild populations.

Some questions we try to investigate :
  • Are traits and behavioural tactics related to fitness, to reproductive success? And if they are, how are they transmitted?
  • What is driving reproductive isolation between individuals, populations, lineages, and species?
  • How can salmonid species have so many problems in their original geographic range, but fare so well when introduced in the southern hemisphere?
  • Can climate change play a major role in these dynamics?

Our experimental channel for salmonid reproduction.

But because these are classical concerns, often addressed by very bright people elsewhere, we also investigate some other questions of more local interest such as:
  • Assuming your genes don’t matter, what sex would you choose to be, and why?
  • Mating with your kin – is it really a problem?
  • Should you eat your children? What if you’re really, really hungry?

A controlled experiment to measure metabolic rate in alevins.

Well, the internet recently arrived in the Basque Country, so we are now happy to announce a new blog dedicated to these questions of utter importance:

The Fish&Bits blog!

Come and visit us!

A view of Kerguelen sub-Antarctic ecosystems monitored by our lab.


(1) Cardoso, S., Valverde, L. Alfonso-Sanchez, M.A., et al. 2013. The Expanded mtDNA Phylogeny of the Franco-Cantabrian Region Upholds the Pre-Neolithic Genetic Substrate of Basques. PLOS One, 8:e67835.

(2) Cavalli-Sforza, L. L., Menozzi, P. & Piazza, A. 1994. The History and Geography of Human Genes. Princeton Univ. Press, Princeton, NJ.

Monday, March 3, 2014

Carnival of Evolution #69

The 69th Carnival of Evolution is now up.  Our contribution to the Carnival is Zach Gompert and Patrik Nosil's post, ‘Experimental genomics’ reveals selection’s role in genome evolution.  Check it out!

This edition of the Carnival celebrates Darwin Day, so let's just end with a picture of the man himself.  Happy birthday, Darwin!  (February 12th, almost a month ago, but the wheels of academia turn slowly, as you knew all too well.)

Darwin as a young man.

A 25-year quest for the Holy Grail of evolutionary biology

When I started my postdoc in 1998, I think it is safe to say that the Holy Grail (or maybe Rosetta Stone) for many evolutionary biologists w...