Friday, March 24, 2017

Roads go ever ever on

As a grad student—at a time when journals were rapidly disappearing from print in favor of online-only formats—I set two pseudo goals for myself: one was to publish a paper (period!) in an actual, printed journal, and the other was to have a paper featured on a cover. As a tremendous amount of luck would have it, Jonathan Richardson and I recently managed to pull off this feat. This past month, in a paper in Frontiers in Ecology and the Environment, we advocate for evolutionary perspectives in the ever-growing field of road ecology.

Roads as drivers of evolutionary change! With a paper hot off an actual press and featured on a cover, the author of this post is overly giddy to tick off two bucket list items.

The motivation for this paper (besides our personal view that road-induced evolution is really fascinating and probably pervasive the world over) is that evolutionary perspectives have generally been lacking in road ecology. While road ecologists have furnished a wealth of knowledge about the vast suite of road effects impacting the planet, insights into evolutionary consequences have typically been overlooked. And from what we can tell, that vast suite of effects is a recipe for evolutionary change.

But before we dive into the topic of road-induced evolution, let's first consider why roads matter from a conservation perspective. As always, it seems prudent to turn to a passage from Tolkien for an inspiring prelude. Thankfully, in The Hobbit, Bilbo Baggins returns from his journey singing a song about roads:

       Roads go ever ever on,
       Over rock and under tree,
       By caves where never sun has shone,
       By streams that never find the sea… (Tolkien 1938)

True to form, Tolkien's words speak as much about present day as days of yore. Roads most certainly do go ever ever on, and indeed can be found among the most remote and picturesque places. Said to be the largest human artifact, roads traverse some 64,000,000 km across the planet. When we consider the numerous negative ecological effects caused by roads (see below), it is easy to see why this global network of pavement and dirt has earned the nickname 'the giant embracing us'. 

The global road network -- an intertwining matrix of highways and byways -- is well described by its (underutilized) nickname 'the giant embracing us'.

In the United States (which hosts about 10% of the global road network), one percent of the landscape is occupied by road infrastructure. At first blush, this may not sound like much; after all what could one percent really amount to? Well, in this case, quite a lot. In terms of shear magnitude, this one percent constitutes 14,000,000 lane km of roads. Said another way, the U.S. has enough road materials to pave a 25-lane highway (with a 12-lane unpaved shoulder) from here to the moon.

In the United States alone, there are enough roads to pave a 25-lane highway (and 12-lane soft shoulder) from Earth to the Moon.

Across this massive network, roads cause numerous, negative ecological effects. From road kill to contaminant laden runoff to fragmentation effects; from the spread of invasive species to the spearheading of land development to impacts on gene flow; roads are something of a one-stop shop for human impacts on the environment.

Among the various ways we utilize and modify the landscape – from agriculture to urbanization to forest harvest – roads are rather unique in that their effects are far-reaching despite having a relatively small footprint. Indeed, road effects extend well beyond the road surface and verge. For example, in the United States, that one percent of the area covered by roads is estimated to ecologically influence 20% of the landscape.

Roads are also unique in that their impacts can be substantial in ares that are otherwise undisturbed. Whether in contexts of highways bisecting large tracts of undeveloped land between distant destinations, or forest roads zigzagging through protected landscapes, roads and their impacts can be found among the most beautiful places on the planet. Indeed, while the impacts of roads may seem obvious in urban places, the aesthetic of our beloved country roads may belie their insidious nature (sorry, John Denver). All of this is to say that there are an awful lot of roads out there causing an awful lot of ill effects in an awful lot of places.

Road effects are many. And many of those effects likely act as agents of natural selection (making roads ripe for evolutionary study!). 

Before I go any further on this road-bash, I have to make a confession: I love roads (and John Denver, just to be sure). As much as there is to hate about roads and their nasty ecological effects, there are easily as many things to love about them. Roads are the great journey-makers, the great soul-soothers, the great inspirers. Roads welcome all traveler alike. Roads do not judge, they do not play favorites, and they rarely let us down. Roads have shaped our economies, our cultures, and arguably our collective conscience. I might even go so far as to say that roads are the veins on the planet through which we humans course—with all of our hopes, dreams, and love.

Personally, I’ve put more miles on my cars than the ecologist in me cares to admit (although decidedly fewer miles than the road-tripping climber in me would prefer). Few feelings can compete with the first glimpse of an iconic destination after hours or days on the road. Whether rounding the corner to that first view of a massive granite cliff or cresting a hill to that first sight of the ocean, roads are a path to something that resonates deep inside us. Roads can also be great places to think. I find few things as mind-cleansing or idea-provoking as a long, quiet drive (or a bike ride for that matter). Undoubtedly (and surely out of necessity at times), some of my best ideas have come to me on long drives.

Yet another hazard of roads: the out-the-window selfie. The author, boat in tow, blazes across the country for the umpteenth time, chasing the sun, the open road, and the promise of possibility that lies ahead. 

Long before roads appealed to my adventurous side (and about the time when my siblings and I lived in fear of the phrase 'scenic route'), I was struck by the potential for roads to impact nature. I can remember the uneasy feeling I would get as a child watching a plow truck pass by, leaving a blanket of salt in its wake.

At that time (mid 1980s), ecologists had not paid much attention to road effects. In fact, despite the long history of roads on our landscapes, it was not until the mid 1990s that the ecological impacts of roads drew the eyes of many ecologists. As the story goes, it was 1994 when Richard T. T. Forman (the 'father of road ecology') was driving to the annual ESA meeting (via the scenic route, no less!). On that fateful drive, Forman—impressed by the scale of the canyon road before him—envisioned the critical need for an ecological understanding of road effects. (A perfect example of what roads can inspire!)

Contrasting Forman's vision, the ESA meeting left him disappointed: of the more than 2000 presentations that year, only one had the word ‘road’ in its title. This disappointment was apparently converted rapidly into inspiration and action. Less than a decade later, Forman and colleagues had amassed enough information on the ecological effects of roads to write the formative book on the subject (Forman et al. 2003). Since that time, the field has advanced steadily, unveiling the diverse ecological consequences of the net of roads blanketing modern landscapes. Road ecology institutes have formed, reviews have been published (e.g. Formanand Alexander 1998, Trombulak and Frissell 2000), and practical guides have been written (Andrews et al. 2015, van der Ree et al. 2015). Yet amid this wealth of knowledge, one insight remains conspicuous by its absence; namely, evolutionary change caused by roads. Indeed, my experience at a recent ESA meeting left me feeling disappointed much like Forman; among the dozens of talks on road effects, only one mentioned evolution.

The field on road ecology has grown steadily since its inception in the 1990s (inset). While many effects are well described, road ecologists have only scratched the surface of evolutionary consequences of roads.

This absence of the evolutionary consequences of roads is surprising for a couple of reasons. First, other contexts of conservation have been hot on the trail of human-induced evolution for some time now. And second, some of our earliest knowledge of human induced evolution was actually discovered in roadside habitats. Studies by Briggs (1972), Wu and Antonovics (1976), Atkins et al. (1982), and Kiang (1982) all demonstrated rapid, adaptive evolutionary responses to road runoff contaminants (road salt and lead). Strikingly, all of these studies occurred back in the 1970s and early 1980s! But as far as we can tell, there was little evolutionary road activity after this early group of studies.

Until now. In 2013, Brown and Bomberger Brown reported that during a 30-year period, the number of road-kill cliff swallows decreased despite an increase in overall population size. At the same time, wing length of road-kill swallows increased while that of the overall population decreased. Together, these patterns suggest an evolved response to selection favoring increased maneuverability and vertical takeoff achieved by shorter wings.

At about the same time as the cliff swallow paper, I was finding evidence in my own work suggesting that roadside populations of amphibians were evolving in response to road-adjacency and road salt. In reciprocal transplant experiments, roadside spotted salamander populations showed a local adaptation pattern whereas roadside wood frog populations (in the same suite of ponds as the salamanders!) showed a maladaptation pattern (Brady 2013; 2016). From my perspective, evidence for maladaptation in roadside wood frogs was both confusing and surprising (detailed in another Eco-Evo Evo-Eco post), particularly since it occurred in counterpoint to the adaptive response of the co-inhabitant salamanders. 

These outcomes of adaptation and maladaptation occurring side by side are part of our argument for the need to consider evolutionary change in the context of road ecology. In essence, the severity of the consequences of roadside dwelling appear to be decreasing for some species but increasing for others. These contrasting patterns occurring in response to the same form of habitat conversion (ie roads) highlight the complexity induced by road effects that are only unveiled through the lens of evolution.

Our goal in writing this paper is to advocate for a new way of thinking about road effects. It is our hope that questions aimed at understanding road effects will be guided by a recognition of the evolvable nature of populations, both in adaptive and maladaptive directions. Indeed, shortly after our paper was published, I was heartened by an influx of emails by researchers who were prompted to share their anecdotal evidence of evolutionary change in a variety of roaded contexts. If those emails any indication, we appear to be on the right track toward our stated goal of shifting gears in road ecology. Hopefully, road ecology will soon yield insights into adaptation and maladaptation across suites of species and contexts, the genetic variation underlying those responses, and the likelihood for adaptive versus maladaptive outcomes.

The future of road (evolutionary) ecology is wide open.

As I wrap up this blog entry, something else occurs to me. That is, this call to shift gears should go out not only to road ecologists, but also to evolutionary ecologists by and large. So here is my pitch to those researchers already steeped in evolutionary biology: come over to the roadside! Roads are natural (ish) laboratories for studying evolution. The suite of potential selective agents associated with roads is diverse and seemingly strong. And, selection appears to be 'hard' in many cases, where populations decline from pressures such as road kill. Further, as Mary Rogalski keenly points out in a recent Eco-Evo Evo-Eco post, selection from pollution may pose a unique set of challenges compared to more typical forms of selection (such as from predation and competition). Not to mention, roads acting as impediments to gene flow can hasten responses to selection.

All in all, roads are ripe for evolutionary study. Hopefully, a decade from now, we will have a handle not only on the giant's embrace, but also the way that life squeezes back.

Saturday, March 18, 2017

Over-citation: my papers that should be cited less often

Ever write a great paper – an important one – and publish it to great expectations? “Surely everyone will love this paper,” you think. It is going to be a barn-burner. It is going to bust Web of Science – maybe even Google Scholar – with citations. Then, as the weeks and months and years go by, pretty much nothing happens. The paper gets a few citations (mostly from your own group), a few people seem to have read it, but not much else. And you think, “How did this happen”? “That was one of my best papers ever – it should be more widely cited.” Perhaps you start to think, “Maybe folks just missed it. If I could only get it in front of them again, people would recognize its greatness and it would go viral.” So you write a blog about “hidden gems” or you emphasize the paper on your website or you send out a few tweets or all of the above. And …. nothing happens. So you carry a (mild) resentment to your retirement, where you give your “exit seminar” and talk about your great work that just didn’t get the attention it deserved. (Yes, I have seen this happen.) Well, this post is about the exact opposite situation – papers that get way more attention than they deserve.

When one applies for a research grant, one usually has to talk about how wonderful one is – at least partly in relation to publications and citations. This need usually takes one to Web Of Science or Google Scholar to find out numbers of citations and H-indices and so on. Whenever I do this (such as yesterday while preparing a grant application), I see my top cited papers. I look at some of them and think, “Well, yeah, that paper was indeed useful and influential” but, about the same amount of time, I think “What the hell, why does THAT paper have so many citations?” So, I thought I would here take the opposite tack to the usual “papers of mine that should be cited more” and write about “papers of mine that should be cited less.” In doing so, I first need to point out that there isn’t anything wrong with these papers, they simply seem to have received more attention (or at least citations) than their content might deserve – or that we, as authors, expected.

One choice for an over-cited paper might be a short note we published in Conservation Biology about how species distribution models that predict massive extinction under climate change generally ignore evolution and are therefore probably often wrong. Models of this sort look at the abiotic conditions where a species is currently found, ask how the geographical distribution of those conditions is expected to change into the future, and then – if the conditions currently occupied by a given species in a given area shrink excessively – make a prediction of likely extinction. The problem, of course, is that species might evolve to occupy the changing abiotic conditions as selection forces them to do so – which is the only point we made in this paper. This point is certainly correct and many papers have now shown that such modelling is likely to be wrong much of the time, partly because of evolution. Yet it just seems so obvious as to not warrant a citation and – really – all our note did was point out that evolution could be rapid and that it could cause a mismatch between predicted and realized future species distributions. Does this rather obvious insight in a very small note really deserve 200+ citations in 7 years?

And the third most cited paper on Eco-Evolutionary Dynamics is ....
(coauthors redacted to protect the innocent)
Another choice for an over-cited paper might be the introduction we wrote to a Philosophical Transactions of the Royal Society special issue on Eco-Evolutionary Dynamics. The introduction simply pointed out that evolution could be rapid and that evolution could influence ecological process, before then summarized the papers in the special issue. Again, nothing wrong with the paper, but a summary of papers in a special issue is hardly cause for (soon) 300+ citations, nor is that typical of such a summary. I here assume that people are citing this paper mainly for the first two general points we make as listed above. This is fine, but excellent papers that treat eco-evolutionary dynamics as a formal research subject, rather than a talking point, are out there and should be cited more. Indeed, several papers in that special issue are precisely on that point, and yet our introduction is cited more. Similar to this example of over-citation, I could also nominate the introduction to another special issue (in Functional Ecology) – which is my fourth most cited paper (437 citations).

Why are these “OK, but not that amazing” papers so highly cited? My guess is that two main factors come into play. The first is that these papers had very good “fill in the box” titles. For instance, our PTRSB paper is the only one in the literature with Eco-Evolutionary Dynamics being the sole words in the title. Thus, any paper writing about eco-evolutionary dynamics can use this citation to “fill in the citation box” after their first sentence on the topic. You know the one, that sentence where you first write “Eco-evolutionary dynamics is a (hot or important or exciting or developing) research topic (REF HERE)” The Functional Ecology introduction has much the same pithy “fill in the box” title (Evolution on Ecological Time Scales) and, now that I look again, so too does the Conservation Biology paper (Evolutionary Response to Climate Change.) The second inflation factor is likely that citations beget citations. When “filling in the box”, authors tend to cite papers that other authors used to fill in the same box – perhaps partly because they feel safe in doing so, even if they haven’t read the paper. (In fact, I will bet that few people who cite the above papers have actually read them.) One might say these are “lazy citations” – where you don’t have to read anything but can still show you know the field by citing the common-cited papers.

Of course, I too sometimes take the lazy citation strategy. Sometimes when I am busting out an introduction and initially write “This [topic here] is a (hot or important or exciting or developing) research area (REF HERE)”, I simply fall back to my usual set of citations that I haven’t looked at for years and years. Doing so is a quick, easy, and safe way to simply move on to the more interesting stuff that really requires reading papers. Or, if I don’t know what to cite, but I know I am stating a well-known fact, I will simply search for the topic on Google Scholar to see what is most cited and then check the title and abstract to make sure citing it is safe. Perhaps this is a bad scholarship – or perhaps it is clever efficiency in the sense that these citations don’t really matter. They are generally known phenomena that have been discussed before and for which detailed additional reading would simply be a waste of time – so I am not exactly condemning “lazy citations” here.

My final closing point is that numbers of citations to a paper don’t always reflect the originality, importance, and quality of the paper. Sometimes papers are dramatically under-cited given their quality and potential importance. Sometimes papers are dramatically over-cited given their quality and importance. Of course, this point isn’t a new one but perhaps I am making it in a slightly novel way.


1.       Patrick Nosil first pointed out to me the “fill in the box” citation-inflation phenomenon.
2.       While writing this post, I noticed that the Google Scholar link for the Conservation Biology paper doesn’t even list me as an author – irony!
3.       No disrespect to my co-authors on the papers discussed above. In fact, my favorite part of all of the above papers was the collaborative writing efforts they involved. Clearly, we did a great job in the writing!

4.       Of course, I have my own papers that I think are way under-cited, particularly several awesome ones published in PLoS ONE (an analysis here). Check it how Humans are less morphologically variable (within populations) than are other animals and Bear predation drives the evolution of salmon senescence in unexpected ways. (And, no, I didn’t write this post simply to plug these under-cited papers.)

Friday, March 3, 2017

Maladaptation to chemical exposure – what may be happening and where do we go from here?

Guest post written by Mary Rogalski

Industrial, residential, commercial, and agricultural development greatly benefit human populations, but with the unintended and widespread consequence of increasing the release and availability of chemical pollution.  Surface runoff and atmospheric deposition introduce a complex mixture of heavy metals, pesticides, pharmaceuticals, and other contaminants into our water bodies. While some pollutants are regulated in an effort to protect human and environmental health, we have very little knowledge of how pollution exposure affects organisms over the long-term. To effectively manage pollution risk, we need to have a better understanding of these consequences.

Exposure to chemical pollution can have a host of negative effects on organisms, including reduced reproductive output, and at high enough doses, death. Individuals in the wild have been found to vary in their sensitivity to pollution exposure, both within and among populations. Based on these negative effects on individuals and the variation in sensitivity, most evolutionary biologists would likely predict that pollution exposure should select for more tolerant individuals. In other words, populations should be able to adapt to exposure.

This was my hypothesis when I set out to investigate the evolutionary consequences of long-term exposure to heavy metals in Daphnia populations in New England lakes (Rogalski 2017). Daphnia (aka “water fleas”) are tiny crustacean zooplankton that are extremely efficient at grazing algae in lakes but are also pretty sensitive to contaminant exposure. To my surprise, I found the opposite of my predicted trend. Daphnia had evolved to become more sensitive to metal exposure over decades of increasing contamination.

 Image of a Daphnia ambigua mother (approx. 1 mm in length). Photo: Eric Lazo-Wasem
 When I first started to see this result, I thought there must be some mistake. However, the pattern was repeated. I saw the same increase in sensitivity to copper following increasing historic exposure in two different populations, and also in response to cadmium in a third population.  In one lake, thirty years after peak copper levels, the sensitivity remained.

Grey points show copper or cadmium contamination through time. Black points show copper or cadmium sensitivity of individual Daphnia clones hatched from different time periods. LC50 is a measure of acute sensitivity, with lower LC50s indicating greater sensitivity. Further details on the study.

I tried to think of what could explain my unexpected result. Surely adaptation must really be happening here, right? But my study is clearly showing the opposite trend. Perhaps there’s an evolutionary trade off at play? Or some other reason why the populations have not only failed to adapt to metal exposure but also became more sensitive?

Alexander Lake, the study site where Daphnia have become more sensitive to rising cadmium concentrations

While the evolutionary pattern is striking and repeated, at this point I just don’t have enough information to understand the mechanism underlying the pattern. I certainly wouldn’t rule out the possibility that these Daphnia populations are adapting to their changing environmental conditions but just happen to be getting more sensitive to acute copper and cadmium exposure. In particular, I am curious to know if the acute and chronic toxicity responses might be inversely correlated. My assays measured acute toxicity – is it possible that being good at chronic chemical exposure makes a Daphnia worse at dealing with acute exposure? At least one study looked at this question in Daphnia with mixed results, finding no evidence of such a trade-off in response to cadmium, and no obvious pattern in response to copper (Barata et al. 2000).

Yet after having spent a lot of time reflecting on my results, I no longer find the trend so unexpected.
First of all, while maladaptation has received relatively little attention by evolutionary biologists, a metaanalysis by Hereford (2009) suggests that maladaptation happens fairly frequently. Of all reciprocal transplant studies examined in this metaanalysis, Hereford found that local maladaptation (defined as foreign population advantage) happened in 29% of cases. If we see evidence of maladaptation when we expect to see local adaptation nearly a third of the time, my result of increasing sensitivity to metals seems much less unexpected.

My study is not the first evidence of maladaptation to pollution conditions in wild animal populations. Researchers found that barnacles (Balanus amphitrite) in polluted estuarine environments were more sensitive to exposure to an antifouling biocide, copper pyrithione, compared with animals from less polluted conditions (Romano et al. 2010).  Rolshausen et al. (2015) found that Trinidadian guppy (Poecilia reticulate) populations have failed to adapt to crude oil pollution, despite devastating effects of exposure to oil. Also, a PhD student in the lab where I did my dissertation work, Steve Brady, found that wood frog (Rana sylvatica) populations in Connecticut ponds were more sensitive to road side environments in general, and road salt in particular compared with salamanders from forested ponds (Brady 2013). Steve found that there were also some overall fitness consequences of this increasing sensitivity to roadside environments. Interestingly, he found the opposite trend of adaptation to roads and road salt in another amphibian species, spotted salamanders (Ambystoma maculatum), inhabiting the exact same ponds (Brady 2012).

Results from Brady’s 2013 study of wood frogs.
In addition, just because pollution can have fitness consequences, I don’t think we should expect chemical exposure to act like other forces of selection such as predation, parasitism, or changing temperatures. Pollution exposure can also lead to increasing rates of developmental malformations, cause changes in sex ratios, and cause cancer. Some pollutants can bioaccumulate in tissues, including those of offspring. When the cadmium chloride that I had ordered for my toxicity trials arrived in the mail, the hazards listed on the safety sheet sounded pretty scary. In particular, cadmium exposure “may cause heritable genetic damage”. The other metal I studied, copper, has been linked with increasing mutation rates in exposed Daphnia populations. It’s not hard to imagine how some of these toxicological impacts could have accumulating consequences over the course of many generations of exposure.

One thing that is valuable about my study is that it tracks evolution through time. While local adaptation studies have provided valuable insight into how populations have evolved in response to contaminant exposure, we are missing three critical pieces of information. 1) We don’t know how pollution conditions have changed in the past in a given habitat. We can only compare organisms in polluted and unpolluted conditions; 2) we don’t know what the historical evolutionary trajectories of these populations look like; and, 3) in most cases the phenotypic responses that we observe may include genetic, plastic, epigenetic, and/or maternal effects.

In my study, I was able to address these issues. I used lake sediment archives to track both environmental and evolutionary trajectories over time. I measured metal contaminants in dated sediments to put together the history of exposure experienced by these populations over the past century. I hatched Daphnia from resting egg banks buried in sediments from high and low metal time periods. I then tested these Daphnia for sensitivity to copper or cadmium to see if the populations had evolved in their tolerance for these stressors. Since we can raise Daphnia clonally in the lab I was able to minimize any maternal effects that might have been present.

Extracting metals from lake sediments using hot block acid digestion. Photo: Sara Demars
In closing, I’ve come away with two key points from this study. First, maladaptation appears to be fairly common but our theoretical understanding of why it happens is pretty limited. This leaves us trying to explain seemingly counterintuitive results with a bit of hand waving and throwing around terms like “genetic drift”, “trade offs”, and “dispersal rates”. As evolutionary biologists we need to do more to understand what drivers may lead to maladaptation to improve our ability to both explain and predict evolutionary trends. Second, if species as different as Daphnia, barnacles, and wood frogs are becoming maladapted to pollution, we should think critically about the risk associated with multi-generational pollution exposure. How common is maladaptation to pollution exposure, and how does this affect the ability of organisms to adapt to other stressors? In what contexts might we expect to see adaptation vs. maladaptation to a contaminant? Could pollution exposure be having long-term damaging impacts on human populations? Those who oppose pollution regulation focus on the financial costs today, but the cost of inadequate pollution control for humans and other species could be much greater over the long-term.

Daphnia resting egg cases from one of the study lakes. Photo: Eric Lazo-Wasem.

Friday, February 24, 2017

A Tale of Two Thousand Cities - by Charles Darwin

The number of cities in the world depends on how you count but it’s a big number. Brilliant Maps says more than 4000 cities have more than 100,000 inhabitants. The UN says 1692 cities have more than 300,000 inhabitants and 512 cities have at least 1,000,000 inhabitants (totalling 23% of the World’s population). And, hey, helpfully narrows the number of cities and towns down to somewhere between 600,000 and (apparently) 4,784,754,000. No matter how you slice it, I am certain there are 2,000 major urban areas with lots of people in them.

"4,037 cities in the world that have over 100,000 people" SOURCE

Cities change everything for the organisms that live in them. Temperature changes. Noise changes. Available habitat changes. Prey changes. Predators change. Food changes. Pollution. Eutrophication. Invasion species. For years, the temptation was simply to write these areas off from the perspective of biodiversity and nature; but – over many years – a shift has occurred to establish a vigorous field of “urban ecology”. The idea is that cities are ecosystems too and we should manage them and their biodiversity as such. And where ecology goes, evolution follows. That is, any sort of environmental change is expected to impose selection on the organisms that remain in that environment, which should lead to evolutionary adaptation to urban environments. This post is about how urbanization dramatically shapes the evolution of many species. I might have called it “Darwin Comes To Town” but Menno Schlithuizen’s forthcoming book has already appropriated that wonderful title.

The past few decades saw a smattering of studies demonstrating evolution in response to urban environments. Byrne et al. (1999) showed that a new form (species?) of mosquitoes had evolved in the London Underground. Cheptou et al. (2008) showed that plants evolved reduced dispersal in cities because dispersers were likely to end up in the in hospitable “concrete matrix.” Following from these earlier, somewhat sparse demonstrations, studies of urban evolution have really heated up recently: cool new papers are coming out, books are being written, grants are under review, symposia are being organized, and working groups are being convened. Inspired by this recent enthusiasm, I want to highlight some of my own work in this area, some of the exciting new work that has come out this year, and some attempts to tie it altogether through meta-analysis.

Darwin's finches of multiple species near Puerto Ayorra pigging out on rice provided by humans. 

My own foray into urban evolution started with coincidental discoveries in Darwin’s finches of Galapagos. Up to the 1970s, medium ground finches (Geospiza fortis) at Academy Bay, beside the small town of Puerto Ayora on Santa Cruz Island, were bimodal in beak size: many large or small birds with relatively few intermediates. By the time we started working there in the 2000s, Puerto Ayora had grown dramatically, and the collection of new beak size data did not reveal the same bimodality as in the past. Yet at the same time, we uncovered bimodality at a site (El Garrapatero) well removed from the town where finches were not exposed to urban conditions. Compiling data from 1964 to 2005, we confirmed that beak size bimodality was lost the finches living in and around Puerto Ayora coincident with the dramatic human population increase. We then showed in later work that this collapse of diversity was associated with a degradation of the diet differences that normally differentiate the species. In short, all the finches are now feeding on human foods, which has removed the selection pressures formerly favoring diversification in this group. Indeed, additional work we currently have in review shows that urban finches are actively attracted to humans and their foods, whereas finches outside of the city are not.

Darwin's finch beak size distributions, with the arrow showing situations tending toward bimodality.

Acorn ant colonies are entirely contained within acorns, which is pretty darn cool – and makes for a wonderful experimental system. One can pick up an acorn and move it to a new site, or to the lab, and thereby test for thermal tolerances and local adaptation. And – conveniently for the question at hand – oak trees producing lots of acorns are found both inside and outside cities. Sarah Diamond and colleagues tested whether urban acorn ants had different temperature tolerances than rural ants. Consistent with the “urban heat island” effect (temperatures are higher inside cities than outside), the authors found that city acorn ants had higher thermal tolerances, and that this difference could be attributed to a complementary combination of plasticity (warmer rearing temperatures increased thermal tolerance) and genetic differences (city ants had higher tolerances for a given rearing temperature). But the temperature effects of cities might not always be so straightforward.

From Diamond et al. (2017)

One of the most ubiquitous plants in urban environments is clover – as a kid, I spent many hours searching for 4-leafed versions. Clover is also abundant outside cities, and so might be a good model for understanding how evolution proceeds in response to urban conditions. Marc Johnson, Ken Thompson, and colleagues hypothesized that the urban heat island effect should lead to the evolution of reduced freeze tolerance in clover, which is controlled by a known genetic polymorphism for hydrogen cynanide. Surprisingly, they found exactly the opposite – freeze tolerance genotypes were more common inside Toronto than outside. The same result was obtained for New York and for Boston, whereas no pattern was evident for Montreal. After a long trip down the rabbit hole, the authors showed that, because snow cover is less common in cities than without, some cities are actually “urban cold islands” in winter that favor the evolution increased – rather than decreased – cold tolerance in plants. (Montreal has so much snow both in and out of the city than it doesn’t matter.)

The use of multiple urban-nonurban gradients, as above, allows greater insight than only a single gradient. Also this year, Liam Revell, Kristin Winchell, and their collaborators studied Anolis lizards on Puerto Rico, comparing those in three cities to those just outside the cities. In forests, these lizards are commonly found on branches that can be quite narrow, whereas in cities they tend to occur on the much broader substrates of walls. Previous work showed that hindlimb length tends to evolve according to substrate size – being longer on broader substrates. That was just what the authors found here: city lizards have longer legs and a common-garden rearing environment confirmed that at least some of this difference was genetic.


The above examples are just a few studies from this year. Many other studies are also demonstrating trait responses to urbanization, although, in some cases, it isn’t yet clear if the change is genetically based. City birds sing different songs, appear smarter, have different behaviors and stress responses, sometimes have different clutch sizes, and so on. City mice differ in key genes that might reflect adaptation, Daphnia evolve to be smaller in urban ponds, and so on. These wonderful examples of phenotypic changes (at least some evolutionary) in urban environments raise the question: are they exceptional? Humans influence evolution in all sorts of contexts apart from cities (hunting/harvesting, fragmentation, climate change, pollution, eutrophication, invasive species, etc.), as we recently reviewed in a special issue of PTRSB. Are urban environments any different, such as by driving faster rates of change than in other contexts?

Marina Alberti has led the recent charge in reviewing work on urban evolution and contacted me with an idea to use our database of rates of phenotypic change to quantitatively ask if changes were greater in cities than in “natural” or other human-disturbance contexts. The same database had previously been used to show that – among other things – human disturbances accelerated rates of change, that the most dramatic effects were evident when humans acted as predators, but that evolution was not exceptionally rapid in the context of invasive species. Georeferencing all the observations in this database and linking them to urbanization estimates, the study – a collaboration among many people – showed that adding information on urbanization substantially improved the ability to predict rates of change – a number of which are confirmed to be genetically based. I speculate that the main reason is that urbanization is associated with many forms of environmental change occurring all together (a subset are listed at the outset of this post), which should impose particularly strong and diverse selection on the organisms that persist.

Locations of rate data used in our analysis.

The next time you walk through a city, take a look past the steel, glass, and concrete, to see the plants and animals that live there. (And, of course, to not see all the microbes.) Each of these organisms is experiencing selective pressures that simply didn’t exist in most places until relatively recently. Selection is the engine of evolution and – indeed – many of these organisms have evolved to better suite them for urban conditions. Indeed, some of those organisms might not exist in cities were it not for adaptive evolution keeping pace with increasing urbanization.

Urban evolution is the new hot Broadway (and off-Broadway) play in the evolutionary – and eco-evolutionary – cannon. See it now.

Here are some Darwin's finches pigging out in the Baltra Airport, Galapagos.

Saturday, February 11, 2017

On Sabbatical

Sabbaticals might seem a strange thing to students, administrators, politicians, the general public, and – well – everyone who doesn’t take them. A common perception is that professors who take a sabbatical are “taking a year off” – and certainly that sometimes happens. As a result of perceptions such as this, some countries don’t allow paid sabbaticals, some states within countries don’t allow paid sabbaticals, and some particular universities don’t allow paid sabbaticals. In many other cases, only partial support is provided or the time between sabbaticals increases beyond the normal every-7th-year. In this post, I make the case for fully paid sabbaticals every 7th year as the greatest benefit to everyone.

About the above: I started my Eco-Evolutionary Dynamics book on my first sabbatical and finished it on my second sabbatical! Only sabbaticals made it possible. For more see

Teaching (and service) improves

Most people who do not attend university – and even many people at universities – think that what professors are for is teaching (and various committee-style “services”). Certainly, most professors do a lot of teaching, which is how most students know them. So, if the role of professors is to teach, and they don’t teach on sabbatical, then they aren’t doing their job on sabbatical – so they shouldn’t be paid. This logic is precisely why legislators in some countries and states forbid paid sabbaticals. Professors have other important jobs besides teaching and service – and those other jobs (research!) benefit dramatically from sabbaticals. However, I first want to make the point that even teaching benefits from sabbaticals. The main reason is that: “The biggest thing for the professors is they get the chance to refresh themselves and to escape. They come back … invigorated.”

Teaching the same course year after year after year (or even different courses year after year after year) can whittle away at enthusiasm and the motivation to make major improvements. A year away can completely re-invigorate a professor’s motivation to teach, teach often, and teach well. (Part of this motivation comes from the guilt a professor feels when his/her colleagues have to teach those courses for a year.) From my own experience, I definitely feel this benefit is critical. Just this fall – right after my sabbatical – I taught three courses: my graduate class in Advanced Evolutionary Ecology, an undergrad class in Evolution, and our Introductory Biology class. I also took over coordination of the last of these and gave guest lectures in a number of other classes. Teaching was exciting again – fun again – motivating again. I wanted to do new things, exciting things, more things. This sort of excitement and motivation really improves with a year away from teaching.

Importantly, classes rarely suffer from sabbaticals in the sense that most of the classes are taught anyway – just by other professors. Hence, the long-term benefit to teaching does not come with any major short-term costs. Sabbaticals are good for teaching!

Research improves

The primary thing that many professors do is research. In fact, research at many universities is what professors are supposed to spend most of their time doing. This is critical. Universities are not just about the transfer of information and ideas from experts (professors) to trainees (students), they are just as much about the generation of new ideas and new knowledge. Moreover, this generation of knowledge benefits the transfer of knowledge because students respond much more strongly to professors who are speaking from their own experience – and often injecting examples from their own work. And then undergraduate (and graduate) students can become involved in the research and thereby have real “hands-on” training. In my lectures, I specifically emphasize research conducted by McGill undergraduates who were sitting in the same seats as the current crop of students in the class. Research benefits teaching!

Sabbaticals have a HUGE effect on research because they afford the time and motivation to learn new methods, write new grants, publish that backlog of papers, do intensive field or lab work, etc. Some professors travel to places where they can get training in new technologies. Some professors travel to places where they can be close to their field work, or their collaborators, or important infrastructure. Some professors remain local and focus on publishing papers. On sabbatical, professors have the time to think about science, do science, write science, learn science. Sabbaticals are critically important for research success, particularly “taking it to the next level.”

Apparently not everyone (or every study) finds that average research productivity goes up after sabbaticals. This doesn’t mesh with my experience. Some years ago, Keith Crandall was telling me a story about how he was fighting to convince the administration of a university of the value of sabbaticals. Among other things, he showed a graph of his publication rate in relation to the timing of his sabbaticals. When preparing this post, I asked Keith about graph and he was able to recreate it from Web Of Science – showing big jumps in publication productivity with each sabbatical. 

Keith: thanks for the idea and the graph!

I did the same calculations for myself and found the same thing – big jumps in productivity with each sabbatical. Beyond benefits accruing to the professor and the people influenced by his/her research, universities are often ranked based largely on professor research productivity – and these rankings can have major consequences for funding, recruitment, and continued success of a university.

As an aside, you will see another message in the graph – starting a faculty position is often coincident with a big drop in productivity. For all you new profs out there worried about your slow start, take heart, it is only temporary. It takes time to build up a lab and a research program – and this is the case for EVERYONE.

Sabbaticals rule

In summary, sabbaticals are good for everyone involved. Ok, fine, a politician might say, but “we don’t need to pay the full salary – go out and get some yourself.” To those people, I would say: “Sabbaticals when you travel are extremely expensive, particularly if you have a family.” If you don’t provide full pay to professors, they are much less likely to go to new places, which is of great benefit to many. (Of course, a great sabbatical can also be had while staying in the same location.) My own university provides full support for sabbatical every 7th year (or 6 months support after every 3 years) – THANKS MCGILL – KEEP IT UP. However, even then, I lose money. The only way I can make it work is because I can stay almost for free with family in California and, most recently, the wonderful Miller Institute for Basic Research helped fund my sabbatical at UC Berkeley.

So, please everyone, from someone who has now had two sabbaticals, keep full support for sabbaticals every 7th year. Everyone wins – except those countries, states, and universities who don’t have them. 


To be honest, some graduate students might not benefit so much from their professor going away on sabbatical. Physical proximity between a professor and his/her students is more conducive than is skype to progress on their thesis. Of course, skype, joint field work, and visits can help minimize the cost to these students. Personally, I need to be better in this area on my next sabbatical.

Friday, February 3, 2017

Yes, humans influence evolution. Yes, that has consequences for humans!

Some might think it would be empowering to earn the moniker of "world's greatest evolutionary force" where it would seem some superhero can, Superman style, rapidly make something "evolve". Like tossing a common ancestor into a phone booth and out pops all the species of Darwin's Finches. Whelp, the reality is that this might not be such a great thing. What if this greatest evolutionary force might be causing detrimental things to happen such as biodiversity loss? What if this greatest evolutionary force is affecting human society?

Well, what might this greatest evolutionary force be? For better or for worse, it's humans. For most of us living in our privileged world with a roof over our heads and food in our stomach, it is easy to become ensconced in our little bubble of consumables and disposables while hiding behind some electronic device, and not think about how we, humans, are affecting evolutionary processes. For example, when something is domesticated for human consumption, be it crops or pets, what happens when those domesticated individuals intermix with wild individuals? What happens when we put antibiotics into the wild? What happens when we want to put taxidermy heads on our walls? What happens when we move something from one place to another, intentionally or by accident (does it matter?)? So, perhaps it's time to come out from behind your screen to think about these questions.

All of these questions are important, but it is not enough to just ask how we are influencing evolution, but to also ask what are the consequences of this? How is this feeding back on to humans and our societies? Well, in working with Andrew Hendry from McGill University and Erik Svensson from Lund University, we set out to agglomerate a special issue of Philosophical Transactions of the Royal Society - B focusing on just this question. We came up with the unimaginative, but descriptive title of "Human Influences on evolution, and the ecological and societal consequences".

We structured this issue in a slightly different way where we considered individual contexts of human influence as a 'topic'. These topics include things such as domestication, habitat fragmentation, hunting, urbanization, medicine, disease, and more. For most of the topics, we opted to have two manuscripts related to the topic: a review type article, focusing on a particular context, how that affects evolution, and then in turn, how this might affect humans, and an empirical paper that set out to test some of the ideas laid out in the review.

We considered everything within two theoretical frameworks. The first is the phenotypic adaptive landscape, where a three dimensional surface is pictured with the peaks representing high fitness phenotypes and the valleys representing low fitness phenotypes. Selection would then be acting to push a population up the adaptive peak. If that landscape is altered (say by humans introducing a novel predator), however, then the landscape, and thus selection will shift. Eco-evolutionary dynamics would then consider that change in a distribution of phenotypes and how that would affect the ecology of that population, including changes at the community and ecosystem level.

 As you can imagine, trying to understand how everything is connected can be rather confusing, so we modified the "traditional" eco-evolutionary framework to incorporate all the different parts together.

Using this, we then set out to try and predict which human influence might have the strongest effects on evolutionary and ecological processes. By no means is what we've done comprehensive, it's merely a tiny stepping stone to fully comprehending the impacts that we humans are having on evolution and how that is feeding back to human society. One of the reasons making predictions is so difficult is because evolution can be influenced by a myriad of factors. For instance, predicting how invasive organisms will respond, as well as how the native populations will respond, are dependent on so many biotic and abiotic interactions, it's extremely difficult to predict if the invasion will succeed, and if so, what will the consequences of it be and then how that would subsequently affect human populations.

Let's take a look at one of our thoughts about human influences on evolutionary processes. Depending on the context, specific components can affect selection itself, or other components of evolution such as standing genetic variation or as we put it, evolutionary potential. In some contexts,  a strong effect is quite obvious - hunting and harvesting are usually size specific, which will result in evolutionary changes in size. However, the hunting can not persist forever at high rates as the population would eventually go extinct. Perhaps more important is our efforts to control for pests or perceived "enemies" because it will result in increased tolerance and resistance, which then means we need stronger/better ways to control the enemies, and then they will again evolve increased tolerance. This perpetual "arms race" could, and has, led to things like superbugs that cannot be controlled with any current medicine.

What about potential ecological consequences as a result of this human induced evolutionary change? If we again consider hunting and harvesting, perhaps we are reducing the population size of or even removing a keystone species. If certain species are targeted, where individuals have a strong role in the community structure, their removal will have obvious cascading effects. For example, otters are essential in maintaining the giant kelp ecosystem in the Pacific Ocean, and the loss of otters in this ecosystem, perhaps due to pollution, then cascades into human society as important fisheries and a carbon sequestration source are subsequently lost.
I just wanted an excuse to post a photo of cute otters. 

In our introductory article, we actually ask a total of eight questions relating to human influences on evolution and the consequences they have on human society. We know you will have opinion and agree or disagree with us, so we would love to hear from you in the comments. In a nutshell, we hope this issue make you realize just how much humans are influencing evolution, and that these human induced shifts in evolution have societal consequences. Unfortunately, a large number of those consequences are detrimental to humans. And we're not alone on this planet, so those negative consequences are also affecting everything else!!

Link to special issue:
Link to our introductory article: