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.

Ecology in everyday life: Monday links

To start, it’s reassuring to know that honeybees like caffeine too. So as you sip your coffee, know that you aren’t the only species who benefits from a little something to start the day.

Citizen science success. iNaturalist.org provides a platform for interested citizens to collect and submit observational data for a huge variety of taxa. This creates an expanding database of species IDs and geographical locations across the US. At present, they have 200,000 observations, which is pretty amazing.

Beautiful wildlife gifs, a reminder that nature is an astonishing place.

Predator/Prey. For some ecologists, work and creative undertakings overlap. So with this in mind, I wanted to point out a band that has taken this marriage of art and ecology to the extreme. Predator/Prey is a Canadian band headed by Dak de Kerhove and Adam Phipps that has released an album built around the concept of species interactions. Dak de Kerkhove is a PhD student studying predator-prey interactions between fish with Peter Abrams and Brian Shuter, so in this case art imitates life.

Most of the songs take inspiration from a combination of emotional subtext and ecological theory. For example, “A Run of Rabbits” focuses on prey dynamics and red queen, with the prey ever running to stay in one place. “Plump of Grouse” is inspired by death and predator prey cycles and written from the perspective of a predator. Because de Kerkhove's work has taken him to the far North, the band can't tour, and instead decided to release a web game that allows you to experience predator-prey interactions from the perspective of a fox. Pretty cool.

**The ecological connections are sometimes subtle, so here is the cheat sheet I was given**
Unkindness of Ravens (INTELLIGENCE / MUTUALISM)
Bed of Mussels (ENDURANCE / PASSIVE FORAGING)
Sounder of Boar (REVENGE / LOSS OF TRAITS UNDER DOMESTICATION)
Knot of Snakes (DESIRE / MATE COMPETITION)
Skulk of Foxes (LOSS / MONOGAMY)
Rout of Wolves (POWER / SOCIAL HIERARCHY)
Priory of Panthers (COOPERATION / GAME THEORY)
Plump of Grouse (DEATH / PREDATOR PREY CYCLES)
Mischief of Mice (OVERWHELMED / COMPETITION)
Shoal of Fish (DEDUCTION / CREPUSCULAR FORAGING)
Run of Rabbits (FEAR / RED QUEEN)
Gang of Elk (ACCEPTANCE / SELFISH HERD)
Piteousness of Doves (LOSS / GAME THEORY) 
                           ****

Can you lecture through Twitter?

The question is intriguing, and recently David Shiffman taught a marine bycatch lecture entirely on Twitter. It seems like an excellent way to reach a broad audience and a novel use of social media. I would be interested to know how the participants felt about the content detail. Universities have been diminishing the classroom experience, in favor of online courses, but this Twitter exercise maintains contact with the instructor (as opposed to pre-recorded videocasts with discussion boards monitored by a TA).

Evolution of conservation – what counts?

Winter, M., Devictor, V. and Schweiger, O.. 2013. Evolutionary diversity and nature conservation: where are we? Trends in Ecology and Evolution. http://dx.doi.org/10.1016/j.tree.2012.10.015

and the response:

Rosauer, D.F. and Mooers, A.O. 2013. Nurturing the use of evolutionary diversity in nature conservation. Trends in Ecology and Evolution. http://dx.doi.org/10.1016/j.tree.2013.01.014

The problem has been called the agony of choice – available resources for conservation are dwarfed by need. And as a result, we are forced to prioritize, to save some species and lose others. Much of the attention given to phylogenetics in ecology lately is on its use, questionable or otherwise, in ecophylogenetic metrics. However the important and useful research being done relating evolutionary information to conservation decisions deserves more attention.

This work has created a recurrent and sometimes contradictory discussion about whether evolutionary relationships contribute complementary information to traditional conservation targets (e.g. biodiversity, habitat types) and whether such information can easily be incorporated into conservation activities (e.g. Rodrigues et al. 2005; Faith 2008; Rodrigues et al. 2011; Tucker et al. 2012 etc.). A couple of papers recently in TREE are continuing this discussion and together do a nice job of summarizing the state of evolutionarily informed conservation practices. Most interesting about the article and the response is that even the opposing sides of the discussion appear to be converging on the same conclusion—that evolutionary diversity should be incorporated into conservation decisions—and differ primarily in how they justify this and the extent to which they feel it will be useful.

Phylogenetic diversity (PD) can be defined specifically as a measure of evolutionary diversity, however here it is more generally defined as the evolutionary information (e.g. phylogenetic relatedness) represented in a community and a common measure of evolutionary information. A community with high PD might include many distantly related species and hence represent many branches in a phylogenetic tree. The simplest argument for why PD might inform conservation is that maximizing PD will maximize the range of species’ ecologies and function that is conserved. In contrast, species richness targets have no relation to a community’s functionality.

Although the conservation literature includes many studies of phylogenetic diversity that are oriented towards real-world applications, in practice, conservation activities rarely incorporate PD. Winters et al. seem lukewarm about the value of phylogenetically informed approaches (one header is “A promising but yet ambiguous additional biodiversity component for conservation”). They suggest that there are a number of ways in which phylogenetic diversity can be informative: it can act as a measure of rarity and facilitate decision-making if rarity is a priority (and perhaps other measures of rarity not available) (e.g. http://www.edgeofexistence.org/). It may act as additional information to be incorporated with measures of species richness – areas with similar richness may have very different amounts of PD. However, the authors question “But what would the added value of conserving areas or communities of unexpectedly high phylogenetic diversity, or spending money on phylogenetically eroded areas, actually be?” The most common arguments, they suggest, are that phylogenetic diversity is a proxy for functional diversity and/or a measure of the evolutionary potential of a community. However, since ecological/functional similarity is not always correlated with PD, and evolutionary potential is not related to PD in a predictable manner, these are inadequate.

Winters et al. seem to suggest that PD is valuable because it can (but not always) act as a proxy for things we actually want to account for (rarity, etc). This is the point that the response from Rosauer and Mooers has the hardest time with. Why does evolutionary diversity not have intrinsic value if, say, species diversity does? Further, species richness is objectively a poor measure of diversity, since it treats all species as having equal value. In contrast, phylogenetic measures of diversity already account for one difference (evolutionary distinctiveness) between species, and hence should already be more effective in capturing total diversity in an assemblage. Rosauer and Mooers state “In an era of triage, difficult decisions are being made, and we know that inclusion of [evolutionary diversity] could make a substantial difference to the outcome for biodiversity, suggesting that it should be considered as one among many criteria”.

Regardless of differences in motivation, both authors agree that the greatest barrier is actually in bringing these ideas into practice. There are many ways of measuring evolutionary diversity (and species diversity, if we’re being fair) and choosing the correct metric can be a minefield. Calculating measures of evolutionary relationship requires specialized knowledge. On the other hand, it is easier and faster than ever to generate phylogenetic trees using DNA sequence databases and available software. Further, evolutionary information lacks the attractiveness that taxonomic-focused conservation has (it is more exciting to save the tigers than the genes). So what remains is to make the jump from theory and case studies to practice, and to find ways to explain why an echidna should receive more protection than all the other rodents. But if evolutionary information makes the agony of choice a little less, it is a worthy goal.

The power of phylogenies?
(Lanna Jin)

Cited
Faith D.P. (2008). Threatened species and the potential loss of evolutionary diversity: conservation scenarios based on estimated extinction probabilities and phylogenetic risk analysis. Conservation Biology, 22, 1461-1470.
Rodrigues A.S.L., Brooks T.M. & Gaston K.J. (2005). Integrating evolutionary diversity in the selection of priority areas for conservation: does it make a difference? In: Phylogeny and conservation (eds. Purvis A, Gittleman JL & Brooks TM). Cambridge University Press Cambridge, UK, pp. 101-199.
Rodrigues A.S.L., Grenyer R., Baillie J.E.M., Bininda-Emonds O.R.P., Gittleman J.L., Hoffmann M., Safi K. & al. e. (2011). Complete, accurate, mammalian phylogenies aid conservation planning, but not much. Philosophical Transactions of the Royal Society, London, B, 1579, 2652-2660.
Tucker C.M., Cadotte M.W., Davies T.J. & Rebelo A.G. (2012). The distribution of biodiversity: linking richness to geographical and evolutionary rarity in a biodiversity hotspot. Conservation Biology, 25:2.
Vane-Wright (1991). What to protect - systematics and the agony of choice. Biological conservation, 55, 235-254.

Assorted links: predictable evolution, why the US government maybe the best thing for open access, and the lab junk drawer

A few interesting places to start the week. Probably these are worthy of full blog posts, if only I had the time.

A recently published paper in PLOS Biology shows that in multiple experiments, independent  populations of E. coli showed similar processes driving adaptive diversification. That is, similar ecotypes of E. coli arose from different populations, sometimes as a result of the exact same mutations at the same nucleotide position. A really cool result.

Good news on the open access front - the US government revealed a new policy stating that publications from taxpayer-funded research should be made free to read after a year’s embargo. It will remain to be seen how this plays out for most researchers, but it appears to be an important step, and one inline with European policies. It seems like steps made by big governments and universities will ultimately be what will create a new normal in publishing.

Why do biology labs tend to have hoarder-esque tendencies? Even newish labs seem to have a junk drawer of equipment that may or may not work inherited from past tenants, half used primers, ancient samples in a freezer somewhere, and more sharpies that don't work than do. An amusing list of the usual suspects was complied in this comment thread.

Academic ambivalence, part 2: poor prospects

The topic of Caroline's excellent post on why we choose grad school and an academic career seems to be hitting an on-line crescendo. A number of blogs and numerous posts to the ECOLOG listserve have been arguing and lamenting the state of job prospects and the grad school experience in general. What has been lacking is an analysis of the job numbers. In a case of perfect timing, Jordan Weissmann, and The Atlantic, has posted an excellent analysis of the numbers of recent PhDs employed across fields. The general message is: the number of fulltime, permanent jobs waiting for PhDs has been declining. However, the proportion of PhDs taking up post-doctoral postions has not declined (and in fact has increased for many disciplines).

From PhD comics

People in graduate school need to be cognizant of the available options, but it seems that if there is an emerging bottleneck, it certainly is not at the postdoc stage (the proportion of postdocs has not changed recently). Of course, the academic stream is but one option for recent PhDs, and the loss of other opportunities is a serious concern. The graphs in the Weissmann post enumerate full-time jobs, and I wonder how many people are taking up part-time, sessional positions as a way to move forward? Regardless, employment opportunities are changing.

My feeling is that academic institutions should be doing a better job of researching, and presenting viable career options to their graduate students. There are a number of industry, governmental and non-governmental postions out there, but people in academia often have a very limited understanding of these types of positions -where they are, how many are available and what kind of training they are looking for.

Perhaps it is time for graduate programs institute real career training.

Academic ambivalence: why do we want to join the academic pipeline?

(This is inspired by a few related posts, and the ongoing discussion in the comments and elsewhere...
http://deepseanews.com/2013/02/19294/)

At the foundations of the University is the concept of academic freedom, unhindered exploration. At their best, universities are reservoirs for society’s brightest and most creative thinkers, people who might not otherwise have the opportunity to explore their intellectual potential. Despite the worst things we might say about academia, it is a place with unmatched room for the exploration. And as a result, academic positions are in constant demand from bright, thoughtful people.

As every grad student learns, academia’s popularity greatly outstrips the availability of research funding and academic positions. Last year there was a string of articles declaiming graduate school as a mistake, a pyramid scam, and an institution in drastic need of rethinking. It’s also a place where students interact with like-minded peers for possibly the first time, succeed or fail at independent research, and experience more responsibility for their own success than many full-time employees ever will. Depending on who you listen to, it will be the best, or the worst, experience of your life.

And then there are tenure track positions. These are the holy grail of the academic pipeline. Advertised positions in ecology often get more than 100 applications for a single job. And yet everyone knows that these jobs are accompanied by a list of problems. They are unremittingly--exhaustingly--competitive, and for that reason, they are associated with long working hours and no concept of “overtime”. The frequent moves between universities mean that relationships can be strained or disrupted, the long hours make family life complicated, and women faculty especially face balancing pregnancy and childrearing with academic demands.

And yet. Hundreds of applicants for every position. So this is the ambivalence about academia: is it one of the best jobs in the world or the worst ones? An (admittedly ridiculous) article in Forbes about how faculty jobs are among the least stressful received rapid condemnation. But this must be reconciled against the fact that many professors choose to remain active years after retirement, and that faculty jobs are often ranked among the most fulfilling.

One consequence of this system of concurrent reward and punishment, with its supply of many similarly-talented people and stochastic element, is a strange culture of competitive martyrship. This shows up in many subtle and less-subtle ways on job boards, in personal conversations, on panels and discussions, in the comments on blog posts. The funniest example I’ve experienced was the comment from a grizzled prof that having a dog would decrease my publication output by one paper a year (I can’t imagine how much a baby would set it back). The saddest examples are people who emphasize that they work 12, 14, 16 hours a day, at the cost of seeing their children and/or spouses. These statements are always made with the confidence that this is the necessary sacrifice for success, that people not willing to give up on balance and hobbies and everything else in life are deserving (or at least risking) failure. The people who make these claims are survivors of the academic arms race. They found one strategy (immense hard work combined with talent) that got them through. But this can create the attitude that those not able or willing to sacrifice aren’t deserving of a position – rather than that the position may demand too much of people.

Such people also tend to be more vocal than other survivors of this arms race who had more success balancing the personal and professional. If you are lucky as a grad student, you know some faculty members who had families, hobbies, personal interests, and managed to be successful academics. This suggests that the dichotomy between personal and professional success is not absolutely necessary.

What we really need is less rhetoric and more open debate about what is acceptable and what is appropriate in academia, and how to shift the culture to be aligned with this. This is difficult, but also not impossible. For example, departments can decide that they want to encourage a particular atmosphere within the department. For example, EEB here at the University of Toronto has decided that they want to support families: as a result, there is a move to provide some maternity funding for graduate students, and provide income for faculty on maternity leave to hire a postdoc during this time. The hope is that this postdoc will help reduce the publication gap that having children can cause by maintaining research activities, while also providing support to current undergraduate and graduate students. Obviously this is only a drop in the bucket. But what matters is that we recognize that academia combines both good and bad, and merely selecting for those people who can survive the bad isn’t optimal. Instead, we can try to make academia a place where the best people can thrive. In this I am, and hope to remain, an idealist.

The birds and the bees and the microbes

Vannette et al. 2013. “Nectar bacteria, but not yeast, weaken a plant-pollinator mutualism”. Proceedings of the Royal Society B-Biological Sciences.

"When we try to pick out anything by itself, we find it hitched to everything else in the Universe."- John Muir

You can’t help but marvel at the complexity of ecology, at the intricacy and multiplicity of species interactions. But this complexity is also problematic. For many ecologists, it becomes necessary to focus on a single type of interaction, or on interactions limited to only a few species. But real ecological systems are hardly ever limited to a single important process. They might include competition, mutualism, facilitation, predation, environmental constraints and fluctuations, additive and interactive effects, nonlinearities, thresholds and emergent properties. Can knowledge of  omplexity emerge from simplicity? Can simplicity emerge from complexity? These are important and longstanding questions in ecology, the focus of some of our smartest minds. We may not have the answer yet, but if nothing else, it is helpful when experimental work in community ecology attempts to explore multiple interactions.

For example, some of the work from Tadashi Fukami’s lab is focused on how communities of microorganisms (yeast and bacteria species) assemble in Mimulus aurantiacus nectar. In the past, this work has focused particularly on priority effects and resource competition, which plays an important role in structuring these communities. While past work has suggested the importance of pollinators as a dispersal vector for microorganisms, fascinating new work suggests that microbial communities have important effects on pollinators and their mutualistic interactions with the host plant as well.

Vannette et al. (2013) focused on the effects of the two most abundant species in Mimulus nectar, Gluconobacter sp., an acid-producing bacteria, and Metschnikowia reukaufii, a yeast. They then looked at three related questions – how do nectar microbes affect nectar chemistry, how do they affect nectar removal by hummingbird pollinators, and how to they affect pollination success and seed set. Basically, do nectar microbes disrupt important mutualistic interactions between the plant and their pollinators, or are their effects neutral?

This is where the story becomes interesting. Both types of microbes altered nectar chemistry, but in different ways. The bacteria acidified the nectar (to ~ pH 2.0) far more than the yeast species, and tended to also reduce the sugar content of the nectar far more than the yeast. Hypothesizing that these changes could ultimately affect pollinator preference, the authors then filled artificial flowers with nectar containing either the bacteria, yeast, or no microbes. Half of these flowers were bagged to prevent hummingbird access. Compared to the bagged controls, flowers with bacteria-inoculated nectar had less nectar removed than either yeast-inoculated or sterile nectar. It appeared that nectar removal was related to the changes in chemistry driven by bacterial growth in the nectar. Finally,  the authors looked pollination success in relation to microbial inoculation. Flowers inoculated with bacteria did indeed have less pollination success (measured as the number of stigmas closed) and had decreased seed numbers. Microbial communities were not isolated from the ecology of the plant.

Perhaps none of this is that surprising – hummingbirds are intelligent and will preferentially feed, and pollinator choice is important for plant fitness. However, these bacteria and yeast species are specialized for growth in the hypertonic nectar environment and their continued presence in the ecosystem depends on dispersal from one flower to the next before their host flower dies. The transient nature of this nectar habitat suggests that obtaining a dispersal vector should be important. The fact that Gluconobacter alters nectar chemistry in a way which negatively affects their likelihood of movement to other patches suggests an interesting paradox and a complicated relationship between plants, their nectar microbes, and pollinators. Gluconobacter species growing in Mimulus flowers produce acidifying H+ ions and reduce sugar concentrations in nectar – this increases their likelihood of winning competitive interactions with other microbes in the nectar, which should select for the maintenance of acidifying, sugar-reducing characteristics. But on the other hand, these characteristics reduce the likelihood of being transported to new flowers and persisting in the metacommunity. Further, these pollinator-decreasing characteristics may result in selection by the Mimulus plants for nectar compounds that reduce microbial contamination. So understanding competitive interactions in microbial communities, or understanding pollinator-plant interactions, or understanding pollinator-microbial interactions on their own might be inadequate to understand the important ecological and evolutionary processes structuring the entire system.

Given that the question of simplicity vs. complexity is still so difficult and at least for me, uncertain, I would hesitate to draw a general conclusion about whether this is the kind of work all community ecologists should strive for. But it seems that recognizing ecological and evolutionary context is key, whether you work with Arabidopsis, microcosms, or tropical forests.

Travel the world with the Carnival of Evolution

The latest edition of the Carnival of Evolution, hosted by Lab Rat, is online. Take an evolutionary journey around the world.

Exploring biodiversity science: The BioDiverse Perspectives blog

A network of graduate students has started a new blog called 'BioDiverse Perspectives'. The purpose of this blog is to explore and compile seminal papers in biodiversity science.  In some ways this mode of knowledge gathering replaces existing 'Foundations of...' compilations of classic papers. Instead, this blog creates an ever-evolving dialogue about our understanding of the different dimensions of biodiversity. Check it out!