50 years of applying theory to ecological problems: where are we now?

Fifty years ago, the seminal volume ‘The Genetics of Colonizing Species’ edited by Herbert G. Baker and G. Ledyard Stebbins was published, and it marked a new phase for the nascent sciences of ecology and evolutionary biology –namely applying theories and concepts to understanding applied issues. Despite the name, this book was not really about genetics, though there were several excellent genetics chapters, what it was really about was the collective flexing of the post-modern synthesis intellectual muscles. Let’s back up for a minute.

The modern synthesis, largely overlooked and forgotten by modern course syllabi, is the single most important event in ecology and evolution since the publication of Darwin’s Origin of the Species. Darwin’s concepts of evolution stand as dogma today, but after publishing his book, Darwin and others recognized that he lacked a crucial mechanism –how organismal characteristics were passed on from parent to offspring. He assumed that whatever the mechanisms, offspring varied in small ways from parents and that there was continuous variation across a population.

For more than 30 years, from about 1900-1930, evolution via natural selection was thought disproven. With the rediscovery of Mendel’s garden pea breeding experiments in 1900, many influential biologists of the day believed that genetic variation was discontinuous in ‘either-or’ states and that abrupt changes typified the appearance of new forms. Famously, this thinking lead to the belief that ‘hopeful monsters’ were produced with some becoming new species instantaneously. This model of speciation was referred to ‘saltationism’

Of course there were heretics, most notably the statisticians who worked with continuous variation (e.g., Karl Pearson, and Ronald Fisher) who refuted the claims made by saltationists in the 1920s. Some notable geneticists changed their position on saltationism because their experiments and observations provided evidence that natural selection was important (most notably T.H. Morgan). However, it wasn't until WWII that the war was won. A group of scientists working on disparate phenomena published a series of books from 1937-1950 that showed how genetics was completely compatible with Darwinian natural selection and could explain a wide variety of observations from populations to biogeography to paleontology. These ‘architects’ and their books were: Theodosius Dobzhansky (Genetics and the Origin of Species); Ernst Mayr (Systematics and the Origin of Species); E. B. Ford (Mendelism and Evolution); George Gaylord Simpson (Tempo and Mode in Evolution); and G. Ledyard Stebbins (Variation and Evolution in Plants). With this, they unified biology and thus the modern synthesis was born.

Now back to the edited volume. Which such a powerful theory, it made sense that there should be a theoretical underpinning to applied ecological problems. The book grew out of a symposium held in Asilomar, California Feb. 12-16, 1964[1], organized by C. H.Waddington, who originally saw an opportunity to bring together thinkers on population genetics. But the book became so much more. According to Baker and Stebbins:

“…the symposium … had as its object the bringing together of geneticists, ecologists, taxonomists and scientists working in some of the more applied phases of ecology –such as wildlife conservation, weed control, and biological control of insect pests.”

Thus the goal was really about modern science and the ability to inform ecological management. The invitees include a few of the ‘architects’ (Dobzhansky, Mayr, and Stebbins) and their academic or intellectual progeny, which includes many of the most important thinkers in ecology and evolution in the 1960s and 70s (Wilson, Lewontin, Sakai, Birch, Harper, etc.).

Given the importance of the Genetics of Colonizing Species in establishing the role that theory might play for applied ecology, it is important to reflect on two important questions: 1) How much have our basic theories advanced in the last 50 years; and perhaps more importantly, 2) has theory provided key insights to solving applied problems?

This book is the fodder for a graduate seminar course I am teaching, and these two questions are the focus of our comparing the chapters to modern papers. Over the next couple of months, students in this course will be contributing blog posts that examine the relationship between the classic chapters and modern work, and they will muse on these two questions. Hopefully by the end of this ongoing dialogue, we will have a better feeling of whether basic theory has advanced our ability to solve applied problems.

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[1] See 50^th anniversary symposium

Deconstructing creationist "scientists"

I’ve been fascinated by creationism since I first moved to Tennessee over twelve years ago –home of the Scopes “monkey” trial. And though I’ve been away from Tennessee for about seven years now, creationism still fascinates me. I find it interesting not because their arguments are persuasive or scientifically credible –they’re absolutely not; but rather my interest in it is as a social or maybe psychological phenomenon. Why, in the light of so much compelling evidence, do otherwise intelligent people hold on to something that contradicts the record of life that surrounds us. I’m a biologist because I find the tapestry of life full of wonder and richness, with an amazing story to tell.

But what fascinates me most of all are trained scientists, who hold legitimate PhDs, who take up the cause of creationism. This is interesting from two angles –first the ‘scientists’ (more on them later), and second the organizations that support and fund their operations. Creationist organizations readily adopt and promote these scientist-turned-creationists, even though they routinely belittle and try to undermine working scientists. Its like the Republican party that dismisses the Hollywood elite as not real Americans, but proudly flaunting Chuck Norris or Clint Eastwood. When the PhDs are on the side of creationism, they are great scholars with meaningful expertise, and when they are against creationism (as are 99% of working scientists) they are elitist and part of a conspiracy.

Enter the latest parade of creationist scientists, who’s authority is meant to persuade the public, at a  ‘Origin Summit’ at Michigan State University in a few days. The first thing you see are four bespectacled PhDs, who are authoritized by the fact that they are PhD ‘scientists’. They are: Gerald Bergman, Donald DeYoung, Charles Jackson, and John Sanford. But, unfortunately for them, not all scientists are created equally.

What makes a scientist? That is not easily answered, but education is one element –and having a PhD from a recognized program and University is a good start. But being trained is not enough, there needs to be some sort of evaluation by the broader scientific community. First and foremost, a scientist needs to communicate their research findings to other scientists by publishing papers in PEER-REVIEWED academic publications. Peer-reviewed means that experts on the topic with examine your paper closely, especially the experimental design and analysis, a provide criticisms. All papers are criticized at this stage, but those with especially egregious problems will not be published. Scientists are also evaluated by other scientists when applying for research funds, being considered for promotion (for example, your record and papers should be sent to 5-8 scientists so they can evaluate the meaningfulness of your contributions), or being considered for scientific awards.

Table 1: How to know that you are doing science.

So then, the ability to publish and survive scrutiny is paramount to being a successful scientist. Of course someone who subscribes to science as conspiracy will say: “wait, then scientists control who gets to be a scientists, and so those with new or controversial ideas will be kept out of the club”. The next thing to understand is what makes a scientist “famous” within the scientific community. The most famous scientists of all time have overturned scientific orthodoxy –that is the scientists that were trailblazers and who came up with better explanations of nature. Many scientists appreciate new ideas and new theories, but work on these has to be scientifically robust in terms of methodology and analysis.

Now back to our Origin Summit scientists, how do they compare to normal expectations for a successful scientist? We will use the average expectations for an academic scientist to get tenure as our benchmark (Table 1). First, Gerald Bergman –biologist. He has a staggering number of degrees, some from legitimate institutions (e.g., Wayne State University), and some from unaccredited places with dubious legal standing (e.g., Columbia Pacific University). He had a real faculty position at Bowling Green University but was denied tenure in 1979. He claims that he was fired because of his anti-evolution religious beliefs (his claim –which to me says his creationism cannot be science). He went to court, and long-story-short he lost because he misrepresented his PhD to get a job in the first place. More importantly to our story here is, what was his record? Fortunately for us, scientific publications, like the fossil record, accurately reflect historical events. Looking through scholarly search engines for the period of time between 1976-1980 (when he would be making a case for tenure) I could only find one publication credited to G.R. Bergman, and it appears to be a published version of his dissertation on reducing recidivism among criminal offenders. Published theses are seldom peer reviewed, and this is certainly not biology. He does not meet our basic expectations for the scientific authority he is promoted as.

Next, is Donald DeYoung –astronomer. He is a professor in the Department of Science and Mathematics at Grace College, and Christian post-secondary institution. It has some accreditation, especially for some programs such as counselling and business. Its not fully accredited, but it seems to be a legitimate Christian school. I searched for legitimate peer-reviewed publications, which was tricky because there also exists another D. B. DeYoung, also on the math/astronomy side of the business. If we ignore his non-peer reviewed books, there may be only one legitimate publication from 1975 in the Journal of Chemical Physics, looking at a particular iron isotope –nothing to do with the age of the Earth or evolution. One paper, so he does not meet our expectations.

Third is Charles Jackson with a PhD in education. There is nothing meaningful on this guy to suggest he is a scientist by any stretch of the imagination. Next.

Finally, we have John Sanford, a geneticist. Now we are getting somewhere! How can a person who studies the basic building blocks of life, deny its role in shaping life? He is a plant breeder and was in an experimental agriculture station associated with Cornell University. I found about a dozen real papers published in scientific journals from his pre-tenure time. None are actually on evolution; they seem to be largely about pollen fertilization and transfer, and production of crops. His publications definitely changed later in his tenure, from basic plant breeding to creationist works. Most interestingly, he has a paper on a computer simulator called Mendel’s Accountant, published in 2007, that simulates genetic mutation and population fitness –the basic stuff of evolution, but which can presumably be used to support his theories about mutations causing ‘devolution’ and not the fuel for real evolution. I read the paper. The genetic theory underpinning is not in line with modern theory, and this is further evidenced by the scant referencing of the rich genetics literature. Most of the models and assumptions seem to be made de novo, to suit the simulation platform, instead of the simulator fitting what is actually understood about genetic mechanisms. I assume this is why the paper is not published in a genetics journal, but rather a computer science one, and one that is not listed in the main scientific indexing services (often how we judge a journal to be legitimate). Regardless, of the scientific specifics, Sanford is a legitimate scientist, and he is the one person I would love to ask deep questions about his understanding of the material he talks about.

The one thing to remember is that a PhD does not make one an expert in everything. I have a PhD in ecology and evolution, but I am not competent in basic physiology for example, and would/should not present myself as an authority to a broader public who may not know the difference between phylogeney and physiology.

So, at the end of the day, here is another creationist conference with a panel of scientific experts. One of the four actually deserves to be called that, and even then, he is likely to be talking about material he has not actually published on or researched. There is a reason why creationist organizations have a tough time getting real scientists on board, and instead are relegated to using mostly failed hacks, because there isn’t a scientific underpinning to creationist claims.

Putting invasions into context

How can we better predict invasions?

Ernesto Azzurro, Victor M. Tuset,Antoni Lombarte, Francesc Maynou, Daniel Simberloff,  Ana Rodríguez-Pérez and Ricard V. Solé. External morphology explains the success of biological invasions. Ecology Letters (2014) 17: 1455–1463.

Fridley, J. D. and Sax, D. F. (2014), The imbalance of nature: revisiting a Darwinian framework for invasion biology. Global Ecology and Biogeography, 23: 1157–1166. doi: 10.1111/geb.12221

Active research programs into invasion biology have been ongoing since the 1990s, but their results make clear that while it is sometimes possible to explain invasions post hoc, it is very difficult to predict them. Darwin’s naturalization hypothesis gets so much press in part because it is the first to state the common acknowledgement that the struggle for existence should be strongest amongst closely related species, implying that ‘invasive species must somehow be different than native species to be so successful’. Defining more generally what this means for invasive species in terms of niche space, trait space, or evolutionary history has had at best mixed results. 

A couple of recent papers come to the similar-but rather different-conclusion that predicting invasion success is really about recognizing context. For example, Azurro et al. point out that despite the usual assumption that species’ traits reflect their niches, trait approaches to invasion that focus on the identifying traits associated with invasiveness have not be successful. Certainly invasive species may be more likely to show certain traits, but these are often very weak from a predictive standpoint, since many non-invasive species also have these traits. Morphological approaches may still be useful, but the authors argue that the key is to consider the morphological (trait) space of the invaders in the context of the morphological space used by the resident communities.

Figure 1. From Azurro et al. 2014. A resident community uses morphospace as delimited by the polygon in (b). Invasive species may fill morphospace within the same area occupied by the community (c) or (d)) or may use novel morphospace (e). Invasiveness should be greatest in situation (e). 

The authors use as an illustration, the largest known invasion by fish - the invasion of the Mediterranean Sea after the construction of the Panama Canal, an event known as the ‘Lessepsian migration’. They hypothesize that when a new species entering a community that fills some defined morphospace will face one of 3 scenarios (Figure 1): 1) they will be within the existing morphospace and occupy less morphospace than their closest neighbour; 2) they will be within the existing morphospace but occupy more morphospace than their closest neighbour; or 3) they will occupy novel morphospace compared to the existing community. The prediction being that invasion success should be highest for this third group, for whom competition should be weakest. Their early results are encouraging, if not perfect – 73% of species located outside of the resident morphospace became abundant or dominant in the invaded range. (Figure 2)

Figure 2. From Azurro et al. 2014. Invasion success of fish to the Mediterranean Sea in relation to morphospace, over multiple historical periods. Invasive (red) species tended to exist in novel morphospace compared to the resident community. 

A slightly different approach to invasion context comes from Jason Fridley and Dov Sax, who revision invasion in terms of evolution - the Evolutionary Imbalance Hypothesis (EIH). In the EIH, the context for invasion success is the characteristics of the invaders' home range. If, as Darwin postulated, invasion success is simply the natural expectation of natural selection, then considering the context for natural selection may be informative. 

In particular, the postulates of the EIH are that 1) Evolution is contingent and imperfect, thus species are subject to the constraints of their histories; 2) The degree to which species are ecologically optimized increases as the number of ‘evolutionary experiments’ increases, and with the intensity of competition (“Richer biotas of more potential competitors and those that have experienced a similar set of environmental conditions for a longer period should be more likely to have produced better environmental solutions (adaptations) to any given environmental challenge”); and 3) Similar sets of ecological conditions exist around the world. When these groups are mixed, some species will have higher fitness and possibly be invasive. 

Figure 3. From Fridley and Sax, 2014.

How to apply this rather conversational set of tenets to actual invasion research? A few factors can be considered when quantifying the likelihood of invasion success: “the amount of genetic variation within populations; the amount of time a population or genetic lineage has experienced a given set of environmental conditions; and the intensity of the competitive environment experienced by the population.” In particular, the authors suggest using phylogenetic diversity (PD) as a measure of the evolutionary imbalance between regions. They show for several regions that the maximum PD in a home region is a significant predictor of the likelihood of species from that region becoming invasive. The obvious issue with max PD being used as a predictor is that it is a somewhat imprecise proxy for “evolutionary imbalance” and one that correlates with many other things (including often species richness). Still, the application of evolutionary biology to a problem often considered to be primarily ecological may make for important advances. 

Figure 4. From Fridley and Sax 2014. Likelihood of becoming invasive vs. max PD in the species' native region.

Null models matter, but what should they look like?

Neutral Biogeography and the Evolution of Climatic Niches. Florian C. Boucher, Wilfried Thuiller, T. Jonathan Davies, and Sébastien Lavergne. The American Naturalist, Vol. 183, No. 5 (May 2014), pp. 573-584

Null models have become a fundamental part of community ecology. For the most part, this is an improvement over our null-model free days: patterns are now interpreted with reference to patterns that might arise through chance and in the absence of ecological processes of interest. Null models today are ubiquitous in tests of phylogenetic signals, patterns of species co-occurrence, models of species distribution-climate relationships. But even though null models are a success in that they are widespread and commonly used, there are problems--in particular, there is a disconnect between how null models are chosen and interpreted and what information they actually provide. Unfortunately, simple and easily applied null models tend to be favoured, but they are often interpreted as though they are complicated, mechanism-explicit models.

The new paper “Neutral Biogeography and the Evolution of Climatic Niches” from Boucher et al. provides a good example of this problem. The premise of the paper is straightforward: studies of phylogenetic niche conservation tend to rely on simple null models, and as a result may misinterpret what their data shows because of the type of null models that they use. The study of phylogenetic niche conservation and niche evolution is becoming increasingly popular, particularly studies on how species' climatic niches evolve and how climate niches relate to patterns of diversity. In a time of changing climates, there are also important applications looking at how species respond to climatic shifts. Studies of changes in climate niches through evolutionary time usually rely on a definition of the climate niche based on empirical data, more specifically, the mean position of a given species along a continuous abiotic gradient. Because this is not directly tied to physiological measurements, climate niche data may also capture the effect of dispersal limitations or biotic interactions. Hence the need for null models, however the null models used in these studies primarily flag changes in climate niche that result from to random drift or selection in a varying environment. These types of null models use Brownian motion (a "random walk") to answer questions about whether niches are more or less similar than expected due to chance, or else whether a particular model of niche evolution is a better fit to the data than a model of Brownian motion.

The authors suggest that the reliance on Brownian motion is problematic, since these simple null models cannot actually distinguish between patterns of climate niches that arise simply due to speciation and migration but no selection on climate niches, and those that are the result of true niche evolution. If this is true, conclusions about niche evolution may be suspect, since they depend on the null model used. The authors used a neutral, spatially explicit model (known as an "alternative neutral biogeographic model") that simulates dynamics driven only by speciation and migration, with species being neutral in their dynamics. This provides an alternative model of patterns that may arise in climate niches among species, despite the absence of direct selection on the trait. The paper then looks at whether climatic niches exhibit phylogenetic signals when they arise via neutral spatial dynamics; if gradualism a reasonable neutral expectation for the evolution of climatic niches on geological timescales; and whether constraints on climatic niche diversification can arise simply through bounded geographic space. Simulations of the neutral biogeographic model used a gridded “continent” with variable climate conditions: each cell has a carrying capacity, and species move via migration and split into two species either by point mutation, or else by vicariance (a geographic barrier appears, leading to divergence of 2 populations). Not surprisingly, their results show that even in the absence of any selection on species’ climate niches, patterns can result that differ greatly from a simple Brownian motion-based null model. So the simple null model (Brownian motion) often concluded that results from the more complex null model were different from the random/null expectation. This isn't a problem per se. The problem is that currently interpretations of the Brownian motion model may be that anything different from null is a signal for niche evolution (or conservation). Obviously that is not  correct.

This paper is focused on the issue of choosing null models for studies of climate niche evolution, but it fits into a current of thought about the problems with how ecologists are using null models. It is one thing to know that you need and want to use a null model, but it is much more difficult to construct an appropriate null model, and interpret the output correctly. Null models (such as the Brownian motion null model) are often so simplistic that they are straw man arguments – if ecology isn't the result of only randomness, your null model is pretty likely to be a poor fit to the data. On the other hand, the more specific and complex the null model is, the easier it is to throw the baby out with the bathwater. Given how much data is interpreted in the light of null models, it seems that choosing and interpreting null models needs to be more of a priority.

Evolution at smaller and smaller scales: a role for microgeographic adaptation in ecology?

Jonathan L. Richardson, Mark C. Urban, Daniel I. Bolnick, David K. Skelly. 2014. Microgeographic adaptation and the spatial scale of evolution. Trends in Ecology & Evolution, 19 February 2014.

Among other trends in ecology, it seems that there is a strong trend towards re-integration of ecological and evolutionary dynamics, and also in partitioning ecological dynamics to finer and finer scales (e.g. intraspecific variation). So it was great to see a new TREE article on “Microgeographic adaptation and the spatial scale of evolution”, which seemed to promise to contribute to both topics.

In this paper, Richardson et al. attempt to define and quantify the importance of small-scale adaptive differences that can arise between even neighbouring populations. These are given the name “microgeographic adaptation”, and defined as arising via trait differences across fine spatial scales, which lead to fitness advantages in an individual’s home sites. The obvious question is what spatial scale does 'microgeographic' refer to, and the authors define it very precisely as “the dispersal neighborhood … of the individuals located within a radius extending two standard deviations from the mean of the dispersal kernel of a species”. (More generally they forward an argument for a unit--the ‘wright’--that would measure adaptive divergence through space relative to dispersal neighbourhoods.) The concept of microgeographic adaptation feels like it is putting a pretty fine point on already existing ideas about local adaptation, and the authors acknowledge that it is a special case of adaptation at scales where gene flow is usually assumed to be high. Though they also suggest that microgeographic adaptation has received almost no recognition, it is probably fairer to say that in practice the assumption is that on fine scales, gene flow is large enough to swamp out local selective differences, but many ecologists could name examples of trait differences between populations at close proximity.

From Richardson et al. (2014). One
example of microgeographic adaptations.

Indeed, despite the general disregard to fine-scale evolutionary differences, they note that there are some historical and more recent examples of microgeographic variation. For example, Robert Selander found that despite the lack of physical barriers to movement, mice in neighbouring barns show allelic differences, probably due to territorial behaviour. As you might expect, microgeographic adaptations result when migration is effectively lower than expected given geographic distance and/or selection is stronger (as when neighbouring locations are very dissimilar). A variety of mechanisms are proposed, including the usual suspects – strong natural selection, landscape barriers, habitat selection, etc.

A list of the possible mechanisms leading to microgeographic adaptation is rather less interesting than questions about how to quantify the importance and commonness of microgeographic adaptation, and especially about its implications for ecological processes. At the moment, there are just a few examples and fewer still studies of the implications, making it difficult to say much. Because of either the lack of existing data and studies or else the paper's attempt to be relevant to both evolutionary biologists and ecologists, the vague discussion of microgeographic differences as a source of genetic variation for restoration or response to climate change, and mention of the existing—but primarily theoretical—ecological literature feels limited and unsatisfying. The optimistic view is that this paper might stimulate a greater focus on (fine) spatial scale in evolutionary biology, bringing evolution and ecology closer in terms of shared focus on spatial scale. For me though, the most interesting questions about focusing on smaller and smaller scales (spatial, unit of diversity (intraspecific, etc)) are always about what they can contribute to our understanding. Does complexity at small scales simply disappear as we aggregate to larger and larger scales (a la macroecology) or does it support greater complexity as we scale up, and so merit our attention? 

Ecological processes may diffuse through evolutionary time: an example from Equidae

Body mass evolution and diversification within horses (family Equidae). Lauren Shoemaker, Aaron Clauset. 2013. Article first published online: 5 DEC 2013. Ecology Letters. DOI: 10.1111/ele.12221

One of the things that community phylogenetic approaches have tended to overlook is that how we interpret phylogenetic relationships depends on a model of evolution. For example, the assumption that closely related species also are similar in their traits is implicitly relying on a particular model of trait evolution. One downside to this approach is that different models of evolution may provide different conclusions about macroecological patterns and processes (competition, environmental filtering, facilitation). 

For example, a new paper in Ecology Letters provides an example of how patterns of trait divergence and adaptive radiation can evolve as a result of diffusion evolution, rather than from a single strong ecological pressure. The paper by Shoemaker and Clauset focuses on the Equidae (horse) family, which underwent an adaptive radiation 56 million years ago, resulting in massive increases in diversity and in trait variation, particularly in body size, habitat type and range size, diet, life span and reproductive traits. Several explanations have been proposed for this radiation and in particular the great increase in body size variation (species are estimated to have ranged between 10-1200 kg). A diversity-focused model explains body size divergence as the result of macroecological competition for niches. A limited number of niches at a given size are assumed to be available, and these niches vary in quality or attractiveness. Increasingly extreme body sizes (and presumably less desirable niches) evolve as niches are filled at more desirable sizes. The result is a correlation between diversity and body size variation, much like the one seen in Equidae. The alternative model considered suggests that trait space is filled via diffusion or a random walk, with the only assumption being that there are some physiological constraints – here a hard limit on minimum size, and an assumption of increasing extinction risk as maximum size increases.

From Shoemaker + Clauset, 2013.

Using mathematical models of Equidae body size evoluation, the authors’ results were very clear (figure below): “Using family Equidae as a model system, we found that macroevolutionary ‘diffusion’, in which selective effects on species body size vary independently of the occupation status of nearby niches, explains substantially more of the observed changes in the Equidae body mass distribution over 56 Myr (Fig. 5) than does a diversity-driven mechanism...”. The results are interesting because they are a reminder that the relationship between macroecological patterns (for example, of traits like body size) may be related to evolutionary history in a much more nuanced way than ecophylogenetic studies sometimes assume. Rather, Shoemaker and Clauset suggest that the better performance of the diffusion model--rather than indicating that competition is *not* important--may be effective at capturing many independent ecological interactions and selective effects all driving body size evolution. A macroevolutionary model of competitive effects on trait divergence is may simply be unrealistic, since competition and ecological interactions may be more localized and less generalized in their effects across the entire Equidae family.

From Shoemaker and Clauset, 2013. Left - competition model, Right - diffusion model

“A large role for diffusion does not undermine the general ecological importance of competition, but rather clarifies its role in generating broad-scale patterns for horses in particular, and for evolving systems in general. Macroevolutionary diffusion is an effective large-scale description of many roughly independent ecological interactions and evolutionary constraints on species size variation. Short-term selective effects on size for a particular species can stem from any number of specific mechanisms, including but not limited to competition over ecological niches. So long as the magnitude and direction of these effects, as defined at the species-level, are roughly independent across the taxonomic group, the large-scale pattern will be well described by diffusion. Ecological competition may thus be crucial for individual species, but its effects are more diffuse at the large scale because competition is typically a local process.”

This is a reminder that many phylogenetic hypotheses (trait divergence or convergence in communities, etc) are too simplistic in their assumptions that broad macroecological processes dominating, and instead need to recognize that ecological processes are often numerous, independent, and local, making outcomes more nuanced than usually assumed. 

The evolution of evolution, LEGO in the lab and other Science-y links

My week is coming to an early end as I head off to some friends' wedding tomorrow, so in lieu of another post, here are some interesting science links from around the internet this week :)

This infographic explores how thinking about evolution has changed since Darwin. It shows pretty clearly the circuitous path that science takes, the way ideas converge and diverge, and ultimately become more nuanced and complicated.

A theoretical physicist blogger answers the question "should you write a science blog?". She mentions the basic, but undeniably key points - do you have time? do you really have time? do you like writing? I also like her advice: "don't be afraid of your readers".

Mental illness can be exacerbated or first show up during grad school. Even in liberal academia, talking about mental health issues can be a bit taboo, something that doesn't help anyone. A blog post from Nash Turley considers the issues and implications.

Another serious issue, related to issues of gender in science: an article in the Economist presents evidence that women authors tend to be less cited than male authors, and this was in part due to less self-citation by women.

Also, LEGO now has its first female scientist character, and with her short hair, goggles, lab coat and gloves, she's a great lab safety role model too ;)

Of course, LEGO has many other science-related applications :)

Edit - the link about blogging was initially incorrect, should be correct now.

Evidence for the evolution of limiting similarity in diving beetle communities

Remi Vergnon, Remko Leijs, Egbert H. van Nes, and Marten Scheffer. (2013) Repeated Parallel Evolution Reveals Limiting Similarity in Subterranean Diving Beetles. The American Naturalist, Vol. 182, pp. 67-75.

In 2006, Marten Scheffer and Egbert van Nes published a very nice paper showing the outcome of simulated evolution of competing species. Their results showed how patterns of evenly-spaced clusters of species along a niche axis could evolve to minimize competition via limiting similarity. 

From Scheffer and van Nes (2006): Evenly spaced clusters of species along a niche axis (x-axis) evolved in response to competition.

Within any cluster along the niche axis, species tended to be more similar than expected. The results suggested that complex self-organizing clustered patterns might result from simple competitive limitations. Interestingly, although the original paper suggested that clustered patterns in size distributions are common, only now are these theoretical expectations about the evolution of limiting similarity being tested with data. In fact, though theory has long suggested that patterns of limiting similarity should evolve to allow coexistence between competing species, empirical evidence is rather lacking. Despite this, limiting similarity and competition are staples of ecological thought: for example, patterns of overdispersion in traits or relatedness are often used as evidence for the importance of competition.

The follow-up paper -Vergnon et al. (2013)- tests for the pattern predicted in Scheffer and van Nes (2006) using communities of subterranean diving beetles (Coleoptera, Dytiscidae) in Australia. These species have evolved for over 5 million years in isolated aquifers. If limiting similarity structured beetle communities, the authors predicted that there should be regularity in the spacing of species along a niche axis. If competitive interactions determine species' positions on the niche axis, then their absolute positions on the niche axis could vary between communities so long as their relative positions are evenly spaced. If, in contrast, niches are driven by environmental conditions, species in different communities/aquifers should have similar absolute positions along the niche axis.

The authors used a nice combination of statistics, modelling and observational data (34 communities of beetles representing 75 total species) to test for these predicted patterns. They used beetle size as the measure of niche position, since size is often an indicator of niche position and food availability and identity. For almost all aquifers, co-occurring beetles were significantly different in size. Further, species in different aquifers classified as occurring in the same size classes (small, medium, large), had different absolute sizes (i.e. the largest beetle in one 2-species aquifer was not similar in size to the largest beetle in another 2-species aquifer).  

From Vergnon et al. (2013): Absolute sizes of diving beetles in aquifers with 3 species present. The absolute size in a size class (large - black; medium - white; small - grey) varies between aquifers.

Although the absolute size of species differed between aquifers, the ratio of sizes (regularity of spacing on the niche axis) was highly consistent. Further, simulations of evolution of body size due to competition were capable of reproducing the observed size structure of the diving beetles.

From Vergnon et al. (2013): regularity of spacing between competing diving beetles (measured as the body size ratio). 

This paper does a nice job of integrating theory and data, and combining pattern and process. The focus is on testing contrasting predictions, and the authors use complementary approaches to test statistically for the presence of patterns and to demonstrate with simulations the relationship between the evolution of limiting similarity and the observed pattern. The evidence is suggestive that limiting similarity and not pre-existing environmental niches explains the size structure of communities of competing diving beetles. There are still questions about how far these inferences can be extended. For example, do we expect that predefined environmental niches are really the same across aquifers? How important is competition in these communities - at the moment, the authors only have minimal evidence of gut content overlap from a single aquifer. Further the low diversity of aquifer communities (~1-5 diving beetle species) means that the prediction of clusters of multiple similar species made in the original Scheffer and van Nes paper can't be tested. But the fact that aquifer diving beetle communities have low diversity and are very simplistic is beneficial for the authors. Patterns in diverse communities where multiple processes (predation, migration, etc) are important may be too complex to show clear evidence in observational data. Simple systems (including microcosms) are a good place to find evidence that a process of interest actually occurs. Whether or not that process is important across many systems is of course a more difficult question to answer. 

Why pattern-based hypotheses fail ecology: the rise and fall of ecological character displacement

Yoel E. Stuart, Jonathan B. Losos, Ecological character displacement: glass half full or half empty?, Trends in Ecology & Evolution, Available online 26 March 2013

Just as ecology is beginning to refocus on integrating evolutionary dynamics and community ecology, a paper from Yoel Stuart and Jonathan Losos (2013) suggests that perhaps the best-known eco-evolutionary hypothesis - Ecological Character Displacement (ECD) – needs to be demoted in popularity. They review the existing evidence for ECD and in the process illustrate the rather typical path that research into pattern-based hypotheses seems to be taking.

ECD developed during that period of ecology when competition was at the forefront of ecological thought. During the 1950s-1960s, Connell, Hutchinson and McArthur produced their influential ideas about competitive coexistence. At the same time, Brown and Wilson (1956) first described ecological character displacement. ECD is defined as involving first, competition for limited resources; second, in response, selection for resource partitioning which drives populations to diverge in resource use. Ecological competition drives adaptive evolution in resource usage – either resulting in exaggerated divergence in sympatry or trait overdispersion. ECD fell in line with a competition-biased worldview, integrated ecology and evolution, and so quickly became entrenched: the ubiquity of trait differences between sympatric species seemed to support its predictions. Pfennig and Pfennig (2012) go so far as to say ‘Character displacement...plays a key, and often decisive, role in generating and maintaining biodiversity.’

One problem was that tests of ECD tended to make it a self-fulfilling prophecy. Differences in resource usage are expected when coexisting species compete; therefore if differences in resource usage are observed, competition is assumed to be the cause. In the ideal test, divergent sympatric species would be found experimentally to compete, and ECD could be used to explain the proximal cause of divergence. But the argument was also made that when divergent sympatric species were not found to compete, this was also evidence of ECD, since “ghosts of competition past” could have lead to complete divergence such that competition no longer occurred. This made it rather difficult to disprove ECD.

There was pushback in the 1970s against these problems, but interestingly, ECD didn’t fall out of favour. A familiar pattern took form: initial ecstatic support, followed by critical papers, which were in turn rebutted by new experimental studies. Theoretical models both supported or rebutted the hypothesis depending on the assumptions involved. In response the large literature, several influential reviews were written (Schluter (2000), Dayan and Simberloff (2005)) that appeared to suggest at least partial support for the ECD from existing data. Rather than dimming interest in ECD, debate kept it relevant for 40+ years. And continued relevance translated to the image of ECD as a longstanding (hence important) idea. Stuart and Losos carry out a new evaluation of the existing evidence for ECD using Schluter and McPhail’s (1992) ‘6 criteria’, using both the papers from the two previous reviews and more recent studies. Their results suggest that strong evidence for ECD is nearly non-existent, with only 5% of all 144 studies meeting all 6 criteria. (Note: this isn't equivalent to suggesting that ECD is nearly non-existent, just that currently support is limited. There's a good discussion as to some of the possible reasons that ECD has been rarely observed, in the paper).

From Stuart and Losos (2013). Fraction of cases from Schluter 2000, Dayan and Simberloff 2005, and this study that meet either 4 or all 6 of the criteria for ECD.

The authors note that there are many explanations for this finding of weak support: the study of evolution in nature is difficult, particularly given the dearth of long term studies. The 6 criteria are very difficult to fulfill. But they also make an important, much more general point: character displacement patterns can result from multiple processes that are not competition, so patterns on their own are not indicative. Patterns that result from legitimate ecological character displacement may not show the predicted trait overdispersion. The story of the rise and fall of ECD is a story with applications to many pattern-driven ecological hypotheses. There are many axiomatic relationships you learn about in introductory courses: productivity-diversity hump shaped relationships, the intermediate disturbance hypothesis, ECD, etc, etc. These have guided hypothesis formation and testing for 40 years and have become entrenched in the literature despite criticism. And similarly, there are recent papers suggesting that long-standing pattern-based hypotheses are actually wrong or at least misguided (e.g. 1, 2, 3, etc). Why? Because pattern-driven hypotheses lack mechanism, usually relying on some sort of common-sense description of a relationship. The truth is that the same pattern may result from multiple processes. Further, a single process can produce multiple patterns. So a pattern means very little without the appropriate context.

So have we wasted 40 years of time, energy and resources jousting at windmills? Probably not, data and knowledge are arrived at in many ways. And observing patterns is important - it is the source of information from natural systems we use to develop hypotheses. But it is hopeful that this is a period where ecology is recognizing that pattern-based hypotheses (and particularly the focus on patterns as proof for these hypotheses) ask the right questions but focus on the wrong answers.

Long-term studies of Darwin's finches have provided strong evidence for ECD.

Evolution on an ecological scale

Andrew Gonzalez, Ophélie Ronce, Regis Ferriere, and Michael E. Hochberg. 2013. Evolutionary rescue: an emerging focus at the intersection between ecology and evolution. Philos Trans R Soc Lond B Biol Sci. 368 (1610).doi: 10.1098/rstb.2012.0404 (Intro to special issue).

David A. Vasseur, Priyanga Amarasekare, Volker H. W. Rudolf, Jonathan M. Levine. 2011. Eco-Evolutionary Dynamics Enable Coexistence via Neighbor-Dependent Selection. The American Naturalist, Vol. 178, No. 5, pp.E96-E109.

Ecology and evolution are often treated as connected but ultimately discrete areas of study. Ecological processes are usually the main source of explanation for ecological patterns and  ecologists may ignore evolutionary processes under the assumption that these are most important over longer time scales than are of interest (e.g. speciation). However, there is also an increasing recognition that rapid evolutionary dynamics can contribute to ecological observations. In a time where rapid changes to climate and habitat are the greatest threats to most species, the suggestion that rapid evolution might play a role in extinction prevention and diversity maintenance is an important one.

Increasingly researchers are exploring this concept. The concept of evolutionary rescue (ER), has been particularly championed by Andy Gonzalez and Graham Bell of McGill University. ER results when evolution occurs fast enough to arrest population declines and allow populations to avoid extinction in the face of changing conditions. Changing conditions resulting in maladapted populations should result in population declines followed by extinction. However, if selection for resistant types (which are present in the population, or result from mutations) occurs, population declines can be countered. The result is a characteristic u-shape curve, showing the initial geometric decline, followed by a geometric increase – escape from extinction is then a balance between rates of evolution and success of resistant types compared to rates of population decline.

From Bell & Gonzalez 2009.

The question of whether evolution may have relevance to population declines is not precisely new, but it is especially relevant given we are in a period of habitat changes and extinction. A special issue of Proc B is focused only ER, on the question of its importance, prevalence, and predictability. Many of the articles extend theory, exploring assumptions about the type of environmental change, type and extent of the threat, presence of dispersal, spatial gradients, etc. A few articles attempt the more difficult task of testing for ER in natural systems and assessing its likely prevalence and value to conservation activities. It is an interesting journal issue and a great example of the importance of context in determining when an idea takes off. The theoretical background for evolutionary rescue has existed for many years, but it took the context of climate change (and perhaps the collaboration of an ecologist and evolutionary biologist?) for it to gain ground as an area of ecological research.

Another interesting paper, this one linking evolutionary dynamics with community coexistence, is from Vasseur et al. (2011). In this case, the authors suggest an evolutionary mechanism that could augment coexistence when ecological conditions allow for niche partitioning and that could allow coexistence when ecological conditions lead to competitive exclusion. If species exhibit tradeoffs between traits that are optimal for intraspecific interactions and traits that are optimal for interspecific interactions, evo-ecological dynamics can produce coexistence. Such tradeoff means that a species will be a superior interspecific competitor when rare and a poor interspecific competitor when common. Such a tradeoff creates neatly alternately selective pressures depending on whether a species is common (fitness declines) or rare (fitness increases). This is presented as a theoretical model, but it seems like in a tractable system one could easily test for changes in ecological and evolutionary pressures as predicted by the model.

No one would argue with the conclusion that a closer relationship between ecology and evolutionary biology would be beneficial for both. But in practice this seems to be the exception rather than the rule. "Evolutionary ecology" as it exists is fairly restricted, and if complaints about seminar topics is to provide a hint, most ecologists feel disconnected from evolutionary topics and vice versa. If evolutionary dynamics are relevant on an ecological scale, it seems that we should at least attempt to understand their prevalence and importance in natural systems.

Understanding modern human society through the lens of evolution

Book review of Edmund Russell’s ‘Evolutionary History’

We often think about the ways in which evolution has shaped this world, from the amazing diversity of cichlid fishes in the African Great Lakes, to Australian marsupials that seem to replicate strategies that placental mammals have evolved elsewhere (e.g., Tasmanian tiger and the North American wolf). We even look at our own bodies or behaviors to find evolution’s imprint –why do I have a non-functional appendix attached to my intestine? However, we seldom look to important events in human history to examine the effects of evolution, yet, according to Edmund Russell, human history can be better understood through evolution –like my appendix.

Russell is advocating for a new field of inquiry within the study of human history –namely, evolutionary history. When I first read the book jacket, I must admit that I was skeptical. However, this book makes the compelling case that historians gain a much fuller understanding past events by including evolution. Russell’s main claim is that modern civilization is the product of an evolution revolution. Even Russell’s unremarkable dog “Riley, like all dogs, is a testament to the extraordinary power of human beings to shape the evolution of other species”. While citing dogs may seem like a trivial example, it was coevolution that shaped this relationship. Wolves that were less aggressive and less fearful, which tend to be more puppy-like, found benefits by associating with human groups. Human groups that tolerated the presence of these wolves were likely alerted to approaching threats. Even the fact that dogs bark is a product of this relationship. This evolution revolution can similarly explain the domestication of other animals and plants, and ultimately produces the necessary conditions for permanent large settlements.

An important and intriguing underlying theme of this book is that these evolutionary revolutions are not often the product of conscious effort. We are used to the narrative that highlights humans as selecting individuals and driving the evolution towards some goal. But this would require early peoples knowing what they wanted in the end, having a specific goal. In the dog example, do we really think that early humans thought ‘hey, I would like a poodle’? No, the reality is that canines and human changed with one another producing a mutually beneficial outcome. Even the domestication of many of the earliest crop species likely resulted from lazy and sloppy humans. Lazy because humans probably harvested the easiest, most accessible fruits and seeds –selecting for bigger, easily removed fruits that ripened at the same time. Sloppy because seeds were discarded around settlements. Then that laziness again means we looked to those nearby plants for harvesting. Thus evolution has continually informed the development of human civilization and produced the much of the cultural norms today.

While modern cultures may consciously drive evolution through selective breeding and genetic engineering, we are immersed in an evolving world. Diseases that are resistant to drugs, pest that are immune to pesticides, and commercial fish that are now smaller and reproduce earlier are examples of important evolutionary changes that affect human activities and economics. Russell provides evidence that evolution is in part responsible for the industrial revolution, due to some varieties of cotton evolving particular features.

Taken all together, Russell admirably succeeds in his goal of convincing the reader that evolution has influenced much of human civilization. Moreover, his intended audience of historians should be re-assessing previous explanations of important human events by asking the basic question: how has evolutionary change influenced major changes in human history.

Edmund Russell. 2011. Evolutionary History. Cambridge University Press.