Exploring parasite-induced evolution in Lake Tanganyika cichlids

Last time I wrote this review on what roles parasites might play in ecology and evolution. Here I’m back to summarize the results of a new paper, exploring whether parasites can contribute to a process which is right at the intersection of ecology and evolution: ecological speciation. For this purpose we studied the colourful cichlids from Lake Tanganyika, one of the prime examples of explosive adaptive radiations. We made this choice because parasites are often ignored in explaining cichlid radiations, even though habitat shifts and diet shifts (i.e., two commonly assumed drivers of cichlid radiations) are inevitably associated with shifts in infection risk.

Lake Tanganyika is much older and deeper than the other Great East-African Lakes (e.g. Lake Victoria or Lake Malawi), and lake level fluctuations are thought to influence speciation processes by bringing fish populations into episodes of isolation and secondary contact. We assumed that this not only happens with the fish, but also with their parasite communities. The result would be that different fish populations end up with divergent parasite communities. Local differences in extinction risk and species sorting and local adaptation of the parasites would amplify these differences even more. In fact, under this scenario, major habitat and diet shifts would not even be required to observe differences in parasitism between populations and species.

To test this expectation, we investigated the rock-dwelling cichlid Tropheus. This species lives on algae which it scrapes from the rocks. Allopatric populations are highly diverse in colour, and there are more than 100 colour morphs across the lake. Despite this diversity, all populations are ecomorphologically equivalent – i.e. they all live in habitats with rocky substrate, they all scrape algae, and they all look similar for morphological traits other than colour. Colour itself is believed to play a major role in mate recognition in Tropheus, and hence might be involved in the evolution of reproductive barriers, like when populations of different colours come into secondary contact. However, there is no direct evidence that colour matters for mate choice in Tropheus, and even when it does matter, it might be that is marking something else, such as the condition of the fish or local adaptation – for instance, resistance to parasites.

Tropheus sp. hanging around at Kalambo Lodge, Lake Tanganyika, Zambia (Photo: Pascal Hablützel).

With a 700 km long lake north to south and hardly any of the parasite species described, starting this project on Lake Tanganyika back in 2010 was kind of a challenge. In search of adventure we decided to start at the Congo side of the lake. For this purpose we rented the “Primus”,  a shiny, blue 30 feet vessel which otherwise does not transport scientists, but Primus, the local beer. The vessel came with a complete crew, including a captain, a cook, the helper of the cook, two lookouts, and three local scientists of the “Centre de Recherche en Hydrobiologie” from Uvira. The idea behind all this logistical support was to sail from Uvira in the North to Moba, 450 km south (and back). The previous ichthyological expedition of this scale dated from the 1940’s, so a general update on fish (and parasite) diversity seemed like a useful thing to do. Despite a number of limitations, including barely enough horse power to sail faster than 10 km/h, rebellion armies hindering us access to land, the official army eager to inspect our boat for Primus beer,  too strong anti-malaria pills, and the occasional thunderstorm, we completed the round-trip in about five weeks. 

Our vessel, the “Primus”, not exactly well camouflaged for rebellion armies, at it’s top speed of 10 km/h  (Photo: Maarten Van Steenberge)

Sub-optimal (top) vs. optimal (bottom) sailing conditions on Lake Tanganyika (Photos: Joost Raeymaekers)

Even though the expedition was a great success and refreshed our knowledge of fish diversity (see here), we failed on one point: we hardly found any parasites in the Tropheus populations. As parasites are kind of essential for a project on parasite-driven adaptation and speciation, we decided to try again in 2011 and 2012 in another season and in a logistically less challenging part of the Lake: the Zambian shore. We selected eight Tropheus populations from five different colour morphs along the shore, and screened them for parasites. This time there were lots of parasites, and it turned out that different populations do harbour consistently different parasite communities - especially among populations from different colour morphs. 

Top: Lake Tanganyika with its colourful Tropheus populations. Middle: STRUCTURE plot showing that the red, blue, light-olive and dark-olive colour morphs are isolated genetically. Bottom: neighbouring Tropheus populations show differences in infection parameters for various groups of parasites. The black bars (‘barriers’) indicate significant differences in a single year (dashed bars) or in two consecutive years (full bars). Chilanga and Linangu in the west is crocodile country, and we decided to scare them only in the first field year.

These differences in diversity and magnitude of infection imply that fragmented Tropheus populations experience divergent parasite selection pressures. Parasites might therefore contribute to adaptation and reproductive isolation in Tropheus. It is not yet clear whether this is really the case, or whether parasite communities just co-vary with something else. So, the next step is to test whether Tropheus populations are actually adapted to local parasites communities. If so, several pathways of how parasites could induce or contribute to reproductive isolation could be tested. 

Cichlidogyrus, a flatworm parasite specific to cichlids, and a close cousin of Gyrodactylus. This gill parasite is one of the most common parasites we observed – usually more than 80% of the fish are infected (Photo: Maarten Vanhove). 

Of course, parasites represent only one component of the ecosystem, and allopatric populations of cichlids differ in many other known and unknown parameters. In addition, parasites are very diverse, and cannot be considered as a single selection pressure. The parasites investigated in our study included the community of metazoan macroparasites, which differ dramatically in life cycle (some depend on a single host, some also on intermediate and final hosts) and host specificity (hosts during a given life stage of the parasite might belong to one or several hosts). As a result, their impact on host ecology and evolution might vary quite a bit. Given this complexity, there might be several opportunities for eco-evolutionary dynamics. For instance, one parasite species  might be strongly influencing host biology and contribute to parasite-driven speciation, while another parasite species might only feel the consequences of that. A related complexity is that part of the parasite community can disperse with their hosts. Hence, strong dispersing cichlid species might homogenize their own parasite communities across habitats, and thus, parasite communities might not impose divergent selection at all. We therefore also started comparing immunogenetic adaptation in Tropheus, which is a weak disperser, with Simochromis, a related cichlid species which is a very strong disperser. We will be back on this blog to report the results.

Here is the link to the paper:  http://www.biomedcentral.com/1471-2148/13/41.

Raeymaekers JAM, Hablützel PI, Grégoir AF, Bamps J, Roose AK, Vanhove MPM, Van Steenberge M, Pariselle A, Huyse T, Snoeks J & Volckaert FAM (2013). Contrasting parasite communities among allopatric colour morphs of the Lake Tanganyika cichlid Tropheus. BMC Evolutionary Biology 13, 41.

The ever-enthusiastic people of Congo (Photo: Joost Raeymaekers).

Eco-evolutionary supermodels

Eight years ago in Alaska, Joe Travis gave a plenary address as president of the American Society of Naturalists. He began by posing the whimsical and implausible scenario where the program officer at the US National Science Foundation called you on the phone and said “We have a million dollars for you to spend on whatever research question you want.” Joe then asked the audience if they would take the offer. The answer was dead obvious until then he gave the hitch. You had to work on the organism that NSF specified. You could thus have 100% control of the research question but 0% control of the research organism. Hmmm. Now everyone was thinking, “well what organism is it?” Believe it or not, many people – myself included – were thinking they might say no to a million dollars depending on the research organism.

So Joe gave us an organism. NSF, he said, has decided the million dollars must be spent on research using the pirate perch, Aphredoderus sayanus. A fish, I thought, cool, I can do something with that – but what? Joe then read the species description. “The pirate perch, Aphredoderus sayanus, is a freshwater fish of the Percopsiformes order. This small fish (up to 14 centimetres (5.5 in) TL) is native to the eastern half of North America. It is dark brown, sometimes with a darker band near the base tail.” OK, nothing special – just a typical run of the mill small fish. Then Joe continues “A unique feature of this fish is the forward placement of its cloaca, under the head, anterior to the pelvic fins.” Ah, OK, now I know what to study: why in the hell would a fish poop beside its mouth.*

Besides the pirate perch, the point I most remember from Joe’s talk – and the resulting paper – was that some folks are organism people and other folks are question people. Organism people work on one taxonomic group and study tons of questions in that one group – think Peter and Rosemary Grant working on Darwin’s finches or Jonathan Losos working on Anolis lizards. Question people, by contrast, work on a whole host of taxonomic groups but use each to address the same general question. Of course, an organism focus and a question focus are really two independent axes and so you can also have folks that work on many questions in many taxonomic groups – the dilettantes – and folks that work on a single question in a single taxonomic group – the professionals (apparently this is the official antonym of dilettante).

Taking the organism focus to extremes, we have the so-called “model” organisms: the flies, mice, worms, and Arabadopsises (Arabadopses?) of biology that are well characterized developmentally and genetically, having full genome sequences, transcriptomes, clonal lines, transgenic strains, and the like. This historically exclusive club has recently exploded to the point that we now have lots of “model” organisms. As one example, the threespine stickleback is now a recognized model organism – and one of the few that also have been well characterized ecologically. This explosion of model organisms has led to the desire to somehow elevate some models over others – supermodel organisms, if you like.

So what would be (or could be) an eco-evolutionary supermodel? Last week I was visiting Nancy Emery at Purdue University to give the Karling Lecture, and we had a spirited dinner conversation with her lab on the topic. One of Nancy’s students (Elizabeth Larue) was planning her research topic – cast very generally as the role of adaptation to climate change in shaping eco-evolutionary dynamics. Cool question – but what organism to use? Nancy’s lab works on plants, so Elizabeth has spent some time thinking of various eco-evolutionary model organisms, maybe the evening primrose, maybe goldenrod, or maybe even (if all else fails) Arabadopsis. But, if we are really to pick from scratch the best organism for eco-evolutionary studies, would it be a plant – and what would be the other candidates?

Conversations like this usually don’t get very far before someone brings up Daphnia – in fact, they don’t get beyond hello if Luc De Meester, Nelson Hairston, or David Post are present. Daphnia show very rapid evolution, they are short lived and small (which eases experiments and laboratory work), they are “strong interactors” in the community, they can be propagated clonally, and – most amazingly – they can be resurrected from resting eggs in sediments to directly compare the genotypes from the present to various times in the past. (My favorite is the 2008 Nature paper of Ellen Decaestecker where Daphnia and their parasites were resurrected from several times in the past and cross-infected to show that parasites from a given time period were better adapted to Daphnia from that time period than they were to Daphnia from the past and the future.) Who could ask for anything more of an eco-evolutionary supermodel? And so we decided right then and there that Elizabeth’s thesis should be on Daphnia. And why stop there, perhaps Nancy should give up on plants and just switch to Daphnia for all her work.  

The Emery Lab - Daphnia here we come!

If Daphnia are the true eco-evolutionary supermodel, then perhaps we should all work on them. Not so fast, you might say, we need to study many organisms to determine the generality of any given phenomena. OK, true enough, but that is a cop out – it is like saying that Daphnia really are the best but some other poor sucker should study alewives or guppies or stickleback or cottonwood trees or aphids or evening primrose. The hard question is – are Daphnia really that perfect? Perhaps not. First – and as the plant people are presumably thinking at this point – plants have many of the same properties as Daphnia, including the possibility of resurrecting genotypes from the past. Second, Daphnia are so small that no one can study the fate and success of individuals in nature, whereas one can (sometimes with difficulty) for all of the above organisms. Third, much (but not all) of the evolution studied in Daphnia on short time scales is clonal selection, which is equivalent to studying different species.

But then supermodels aren’t perfect anyway – they just look good, at least to most folks. So maybe Daphnia really is the ultimate eco-evolutionary supermodel, it just has the usual flaws of human supermodels, such as binging and purging, bulimia, bad boyfriend choices, drug abuse, and a limited shelf-life. But then again, we don’t have just one human supermodel – we have a bunch of them that we can pick and choose among to suit our current ad campaign (i.e., Nature submission) or our budget or the flavor of the month. The same should be true for eco-evolutionary models and supermodels and, yes, Daphnia can be one of them – but so too can be alewives and guppies and stickleback and cottonwood trees and aphids and evening primrose. I can’t wait for the eco-evolutionary supermodel swim suit issues in Evolution and Ecology.

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*This species description is from Wikipedia, which then continues: “This placement allows the females to place their eggs more precisely into root masses.” I am skeptical. Why wouldn't other fish do this? And why does having your bum under your chin help you be more precise? Did someone experimentally manipulate anus position and test egg laying precision? The question is definitely worth a million dollars of research.

Mixed-species groups –everything is about predation... or isn’t it?: a hypothesis and field evidence

In many species we can see individuals forming groups, and these individuals can be group members for life or just for specific periods of time. So, what are groups and why do they matter? In order to form a group it is necessary for at least two individuals to overlap spatially and temporally. However, the duration, frequency and structure of these associations can vary considerably. Groups matter in evolutionary ecology because they are major “game changers” of fitness.  In their book “Living in Groups”, Jens Krause and Graeme Ruxton review how forming groups affects fitness; for example, they provide protection from predation and may increase the acquisition of resources (i.e. food, mates and all those things that increase survival and reproductive output). But not everything is great about being part of a group, and costs also come in as part of the bargain. One of the most prominent costs is that there is a bigger chance of getting a parasite from other group mates. To make matters worse, larger groups may also increase the amount of competition among individuals and increased competition may lead to lower resource acquisition and therefore to a decreased ability to mount an immune response. Forming groups, as with so many things in evolution, is all about trade-offs. 

There is another kind of group that has elicited somewhat less attention: mixed-species groups (a.k.a. heterospecific groups). As with any other group we are talking about temporal and spatial overlapping of individuals, but in this specific case it requires that those individuals are at least of two different species. These groups might lead to asymmetric benefits for the participating species (only one of them benefits while the other doesn’t ) and requires the active behavioural choice of at least one of the species. It is in the arguments for why mixed-species groups are formed where we run into some complications. The most frequent explanation is that mixed-species groups provide anti-predator advantages, but the mechanisms through which they provide such advantages are the same as those for single-species groups, which should lead to conclude that there is nothing special about mixed-species groups and most likely that they just happen when there are not enough conspecifics to form a large group of the same species. Still, under some situations where conspecifics are abundant, we find mixed-species groups. Another possibility less explored but with some support, is that mixed-species groups reduce intra-specific competition or enhances the ability of one species to find resources. In this case, the heterospecific characteristic of the group is really what matters. But, why then do we still find mixed-species groups where resources and conspecifics are abundant?

A more interesting hypothesis (to me at least) as to why mixed-species groups are formed is that they provide protection against host-specific contagious parasites. As I mentioned earlier, increasing group size leads to more contact among group members and therefore to higher parasite transmission. So, when parasites do better on a specific  host-species (i.e. they are host-specific), an efficient way to reduce parasite transmission and their growth rate is to form mixed-species groups. The main idea here is that individuals in mixed-species groups, relative to a single-species one, should gain similar advantages in terms of protection from predators while reducing the costs of parasitism. So, can mixed-species groups reduce individual parasite load? Find out here. In a recently published study, we found that infection patterns of two Poeciliid species (Poecilia reticulata and Poecilia picta) infected by host specific Gyrodactylus spp ectoparasites support our hypothesis. Both P. reticulata and P. picta have lower Gyrodactylus prevalence and abundance in the field when they form mixed-species groups than when they are in single-species groups. As these groups are formed in sites where food and conspecific abundance is high, it is unlikely that either improved foraging efficiency or lack of conspecifics explain the formation of mixed-species groups. Independently of the mechanism by which the group is established, mixed-species groups provide an advantage to individuals by reducing parasite loads.

Bloggy worms

Bloggy worms? Why worms? Let’s start this post with a small review. Since its start in 2009, the number of contributions on this blog talking about worms, more specifically parasites, has been skyrocketing:

SEVEN POSTS!  How come nobody else reviewed this before? The narrowness of the field alone is already interesting enough for further investigation. So here we go. The word “parasite” was first posted on this blog by Joost (2010) in a list of potential mating barriers in lake-stream stickleback . Great,  I’m the founder of the field – that’s obviously why I’m reviewing it. By the way, other blogs blogging on parasites were out of the scope of this review, because I anticipated that their main message would be that parasites are everywhere. Which we already know and would probably be confirmed once more by running into a computer virus while surfing to these blogs. Parasite-induced dispersal limitation in silico.

After introducing a new discipline on a blog it always takes a while until some dude picks up the term, adds some drama and generates a hype. Indeed, it took more than a year until Andrew (2012) picked up the idea of parasitism, and blogged about cruel maggots (Philornis downsi) sucking blood out of baby finches in Galapagos. From an eco-evo perspective he speculated that this worm might induce the evolution of resistance or tolerance in finches, which then would impact the population dynamics of the finches. And the hype was born.

Shortly after, Felipe (2012) couldn’t resist blogging about “Parasites, guppies and predation”, explaining that there are reasons to assume that when guppies adapt to predation, they might also have to adapt to parasites. But, as parasites (in this case the ectoparasitic flatworm Gyrodactylus) might as well adapt to guppies (i.e. coevolution),  the relationship between adaptation to predators and adaptation to parasites might actually become weak or invisible. Kiyoko (2012) then tried to be almost as original with her title, “Guppies, predators, and parasites”. She challenged the classical view that coloration in natural guppy populations differs between sites because of different predation pressures, whereas it could be as well other factors, such as – have a guess –  parasitism. An effect of parasites (again Gyrodactylus) turned out to be absent (or hard to detect) in her study, but predation alone clearly could not explain the observed variation in coloration. 

Usually, some people then start posting no matter what to be part of the hype.  The post by Ben (2012) is clearly an example of that, wondering whether  “[...] theory and data have a mutualistic relationship, or a commensal relationship, or a competitive relationship – or is one perhaps even a parasite of the other?” Nice try Ben. But the next wormy blogger was Victor (2012), talking about how parasites affect the success of invasive species by altering competition between invaders and local species, and by influencing the interaction between invasive predators and native prey. Clearly, an eco-evolutionary framework is needed to make progress to the field, he concluded. And finally, and most recently, Christina (2013) demonstrated that the hype is not over yet by continuing blogging on guppies and Gyrodactylus flatworms. She explained why – counter intuitively - guppies in better shape have more worms. It must be the quality of the food at the guppy sports center.

So, seven blog posts out of 109 posts so far, or 6.4% of the content of this eco-evo blog, have been highlighting parasites. I hope I did not miss any. Two posts (Andrew and Victor;  1.8% of this blog) explicitly mention that parasites might be important in the context of eco-evolutionary dynamics.  There are good reasons for that. First, parasites often represent strong selection pressures, in some cases by affecting survival (natural selection), in other cases by influencing mate choice (sexual selection). Strong selection pressures facilitate eco-evolutionary dynamics, as it might cause evolution to occur fast enough to influence ecological processes. When parasites target the same host trait by both natural and sexual selection, host adaptation and speciation might even be accelerated with the help of Harry Potter (i.e., magic trait evolution, for more on this see Ben, 2011. Ben is now cited twice!). An opportunity for eco-evolutionary dynamics would occur when hosts are under such strong selection by one parasite species, that they evolve defenses or avoidance behaviors that have a measurable effect in real time on the infection risk by (and hence the happiness of) other parasite species. 

Harry Potter is not the only fiction which might influence host-parasite interactions. There is also the Red Queen. As already mentioned by Felipe, parasites might be involved in co-evolutionary arms races with their hosts, and these arms races can be considered special cases of eco-evolutionary dynamics. In the case of “Red Queen” dynamics, hosts and parasites are interacting in a feedback loop in which they both need to keep  ‘running’ (i.e., evolving phenotypes) to ‘keep in the same place’ (i.e., maintain population size). An example in the water flea Daphnia can be found here. Such dynamics are not inevitable, but the likelihood increases when the parasites are reasonably virulent, and perhaps when they have no other options. Ectoparasites such as Gyrodactylus flatworms and Philornis maggots might be virulent, but often have other options too. Philornis has a low host specificity, so it can easily start laying its eggs in nests of other bird species, which then dampens their selective impact on single host species. Gyrodactylus species as those on guppies are often highly host-specific, but often successfully trace the weaker host individuals – as suggested by Christina (2013). This way they escape Red Queen dynamics by fighting the battle not at the evolutionary level, but at the ecological level. 

It is about time to quit my job as a reviewer, of course not without stressing that much more blogging is needed to really understand what roles parasites play in the intersection between ecology and evolution. So keep bringing them on, those wormy posts!  And perhaps one day we can write a real review about eco-evolutionary dynamics and parasites. Writing this review also distracted me a bit from the initial reason why I started blogging. I just wanted to parasitize on this blog to advertise a new parasite paper. However, blog readers tend to escape blogger-reader coevolutionary dynamics by clicking on the various links inserted in the text . So, I assume by now you all ran into a computer virus, even though I warned you. That’s why  I will keep this paper for a later post. This will allow you to update your virus scanner, and will allow me to cite my own bloggy worm review.

Eco-evolutionary semantics

What is in a name? Presumably a name should be clear and unambiguous, thereby nicely delineating what it does and does not include. After all, we should call a spade a spade, right? Or is it that simple? Perhaps a spade is instead a shovel or a trowel or a digger or a spud or a geotome. “Now wait a minute,” you might say, quoting Wikipedia: “the words spade and shovel should be held in contradistinction (piercing and digging [spade] versus scooping and moving [shovel]).” “Sure, but,” I might retort, quoting the next line in Wikipedia: “Natural language does not widely follow these prescriptions; it more often treats spade and scoop as contradistinguished subsets under shovel.” Thus, even if a shovel is not always a spade, a spade is often a shovel and, regardless, we can call either the other and still get the job of digging done.

What, then, are eco-evolutionary dynamics? I would venture the following definition: eco-evolutionary dynamics are interactions between ecology and evolution that play out over contemporary time scales, with “contemporary time scales” intended to represent time scales ranging from years to centuries. (See more details here.) This definition is intended to be inclusive, thus providing an umbrella framework for understanding how ecology and evolution interact on short time scales. But it doesn’t satisfy everyone – as I will elaborate below.

Cruising the Netherlands at dusk.

For the past week, I have been at a workshop on “Eco-evolutionary dynamics in a changing world” held in Leiden, Netherlands, at the Lorentz Centre. (Much to the surprise of almost everyone present, we learned on the first day that this was not the guy with the geese – that would be Lorenz.) Organized by Stephanie Jenouvrier, Thomas Reed, and Marcel Visser, the workshop had plenary talks, break-out discussion sessions, and group discussions. These activities were interspersed with ample time for social interaction – call them break-out drinking sessions if you will. Antics ensued.

At one dinner, a group of us decided to form an “Institute of This Table (ITT)” with each of us holding a research chair endowed by one of the others. I can’t remember all the resulting chairs, but I do recall that Richard Gomulkiewicz christened Nelson Hairston the “Dick Chair of Cryptic Dynamics” and Mike Kinnison christened himself the “Hendry Chair of Paleontological Genomics.” (I later gave him two Euros.) Later that night, we ended up at an English bar with a truly amazing collection of Scotch whisky. I tried these out on my palate while Dick tried out his Dutch pick-up lines on Mike Kinnison – stay tuned for the youtube video. On another night we took a cruise through the canals around Leiden. After much debate, Chris Thomas and I agreed to reunite for dinner 36 years hence so that he (I) could gloat over me (him) at having proven (disproven) the predictions from his 2004 Nature paper that “on the basis of mid-range climate-warming scenarios for 2050, that 15–37% of species in our sample of regions and taxa will be ‘committed to extinction’.”

The ITT.

For the first two days of the meeting, most of the arguments – and certainly the most animated ones – were about what eco-evolutionary dynamics are and are not. Here is a restrictive sampling of the many uncertainties.

1. If phenotypic differences have an effect on some ecological variable (such as population size or species richness or nutrient cycling), but you haven’t isolated or confirmed that these effects have a genetic basis, then are you studying eco-evolutionary dynamics? The excluders might argue that, if you haven’t demonstrated evolution, then you can’t say you are studying eco-evolutionary dynamics, and that you would be better off saying eco-phenotypic dynamics or some such. The includers might argue against this precision on several grounds. First, if we go down this slippery slope, then the field of evolution quickly gets much smaller. As Mike Kinnison pointed out, we would have to kick out all of the paleontologists given that none of them has yet proven that the changes they study have a genetic basis. Second, we often know that phenotypic differences have a strong genetic basis even if we haven’t proven it in a particular experiment. This is why the eco-evolutionary pantheon includes those great studies of the ecological effects of alewife divergence, guppy divergence, and stickleback divergence – even though all of those studies used wild-caught fish for the experiments. As some of the perpetrators of those studies were present (Ron Bassar and Mike Kinnison), I was tempted for a vote on whether or not we should – right then and there – drag them out of the room and throw them off the eco-evolutionary island – but then I realized I wouldn’t be far behind. Third, phenotypic plasticity evolves, and so plastic responses in a given generation are the product of evolutionary change in a past generation. In this sense, plasticity is the gift that evolution in one generation keeps giving to future generations. Fourth, it is phenotypes and not genotypes that interact with ecology; genotypes interact with ecology only indirectly through their effects on phenotypes. In short, phenotypes – even without information on genotypes – are an integral part of the eco-evolutionary dynamic framework. (Just as every modern evolution text book has a chapter or major section on plasticity, and numerous examples that focus only on phenotypes, so too should any eco-evolutionary textbook. Of course, investigators should make every attempt to explore the genetic basis underlying phenotypic effects and shouldn’t assert genetic change until they have explicitly confirmed it.)

2. If the ecological variable of interest does not change, then are eco-evolutionary dynamics occurring? The excluders might argue that if no change has occurred, then neither have any dynamics – by definition. The includers might reply that stability itself is likely the product of ongoing evolution. Such cryptic eco-evolutionary dynamics could occur in several basic ways: (a) changes in genotypes cause changes in phenotypes that cause stability in ecological variables, (b) changes in genotypes cause stability in phenotypes that cause stability in ecological variables, and (c) selection causes stability of genotypes that cause stability in phenotypes that cause stability in ecological variables. An example of (a) comes from the work of Nelson Hairston’s group, where changes in the frequencies of two different clones of algae that are differentially susceptible to a predator are necessary to maintain algae population size. An example of (b) comes from a number of studies showing “counter-gradient variation”, such as when environmental conditions (e.g., low food) that decrease growth are offset by evolutionary changes that maintain growth. The phenotype will here remain unchanged only because of evolution. Support for (c) comes from the realization that selection is constantly weeding out maladaptive genetic variation that arises owing to mutation, gene flow, and genetic drift. Without this selection, fitness would decline and the population would soon decline too. Stability is thus driven by the continual action of selection. For all of these reasons, it seems clear that the absence of ecological – or even phenotypic or genetic change – does not mean that eco-evolutionary dynamics are absent.

3. If you haven’t demonstrated a FEEDBACK (e.g., a trait influences an ecological variable that then influences selection on that trait), then are you studying ecological evolutionary dynamics? The excluders might argue that only true feedbacks should be considered dynamics but the includers feel this criterion as too restrictive. First, it is very hard to demonstrate feedbacks even when they are present; doing so usually requires manipulative experiments. Second, feedbacks of one sort or another likely occur in nearly all instances – at least in the broad sense. By this I mean that changes in any trait in some focal organism will likely influence some other organism in the ecosystem and thus have ecological effects. Overall, I would argue that eco-evolutionary dynamics should include all interactions between ecology and evolution, even one-way effects, whereas the term eco-evolutionary feedbacks should be reserved for situations where a feedback (ecology to evolution to ecology; or evolution to ecology to evolution) has been explicitly demonstrated or is explicitly hypothesized.  

4. If the interactions between ecology and evolution are happening only on long scales (e.g., millennia) are they eco-evolutionary dynamics? Hanna Kokko argued that such interactions often occur on quite long time scales, and this is certainly the case. Think of all the ecological and evolutionary changes that depended on the much earlier evolution of photosynthesis.  Although I tend to be an includer in all of the above debates, I will caucus with the excluders. The Oxford Dictionary states that dynamics is “a process or system characterized by constant change, activity, or progress”. This would seem to me to exclude long time scales but, oops, this definition is for its use as an adjective. As a noun, the definition is “a force that stimulates change or progress within a system or process.”  This one seems harder to invoke in order to exclude long term effects. And – after all – the Oxford Dictionary clearly calls only a spade a spade: “a tool with a sharp-edged, typically rectangular, metal blade and a long handle, used for digging or cutting earth, sand, turf, etc.” So do I really have any solid reason to exclude longer time scales from the umbrella eco-evolutionary dynamics? I guess I would hand-wave that interactions between ecology and evolution on long time scales have long been recognized but it is only recently that they have been appreciated on short time scales – and it is this latter appreciation that has driven the emerging field of eco-evolutionary dynamics. This is why definitions of eco-evolutionary dynamics have tended to focus on short time scales and this distinction currently delineates the field. And, after all, who wants to have to say “contemporary eco-evolutionary dynamics” (although CEED sounds cool) or, Darwin forbid, “rapid eco-evolutionary dynamics” (REED?).

So where do these semantics leave us? I would like to suggest that eco-evolutionary dynamics is a FRAMEWORK for understanding interactions between ecology and evolution on contemporary time scales, and it therefore needs to be inclusive. Or, as Hal Caswell pointed out, eco-evolutionary dynamics can be considered a social identifier that places one comfortably into the group of researchers applying evolutionary thinking in ecological studies. I would suggest that this group is inclusive with respect to the first three debates (and many others) but is (arguably) exclusive for the fourth.

These semantic issues largely subsided toward the end of the meeting given that we really could communicate quite clearly without going to further trouble. This left the rest of the meeting to argue over more substantive issues, like whether or not evolutionary (or even ecological) models can reasonably predict what will happen in the future, how important is evolution in nature, can Lande Land accommodate density- and frequency-dependent selection , which deep-fried Dutch croquette was the best (or worst), and how could Heineken simultaneously be the worst beer and the best wine in the same restaurant.

The rise and fall of parallel evolution: dispatches from Belgium and Texas.

Evolutionary biology has traditionally sought support for the power of natural selection through evidence that similar phenotypes evolve in similar environments: flying animals all have wings, cave organisms predictably lose their eyes and pigments, and birds on small islands often lose their wings! If similar traits evolve in similar environments despite independent origins, then surely natural selection is overwhelmingly powerful in shaping the deterministic evolution of organisms. This pattern is generally called “parallel” when it occurs from similar ancestors and “convergent” when it occurs from different ancestors. (Although some interpretations focus more on whether similar [parallel] or different [convergent] genetic changes are involved.) In this vein, countless studies have reported parallel or convergent evolution and thereby provided overwhelming evidence for the power of natural selection.

I will here argue that parallel evolution is – or should be – on the wane. I don’t mean this in the simple semantic sense that evolution is never parallel but is instead convergent; as has been recently argued by a number of authors. I instead mean it in the more subtle, but probably more important, sense that parallel (and convergent) evolution is much less parallel (and convergent) than is normally promulgated – and that evolutionary biologists are increasingly realizing this fact. My inspiration to revisit this topic (see the earlier post) stems from meetings I recently attended in Leuven, Belgium, and Austin, Texas.

The typical approach in studies of parallel or convergent evolution is to test whether independent populations that have evolved in similar environments (or habitats or food types) are more similar than independent populations that have evolved in different environments. If a statistically significant effect of “environment type” is found across such populations, then parallel evolution is invoked. The trouble with using this result to invoke parallel evolution is that independent populations in similar environments, although often superficially similar, do show many subtle (or even obvious) differences. Wings look extremely different for pterosaurs, bats, birds, and insects! Not all cave organisms lose their eyes!  Not all birds on small islands lose their wings! Has our need to invoke the power of selection blinded us to the fact that evolution is not very predictable? Or, in short, how parallel (or convergent) is parallel (or convergent) evolution, really?

Several talks at the Leuven meeting invoked parallelism (or convergence): spiders in Hawaii, spiders in Galapagos, beetles in salt marshes, stickleback in freshwater, and many others. In most cases, however, examination of the data made clear that although all evolution generally occurred in roughly similar directions, the independent populations colonizing similar environments were never the same either morphologically or genetically. That is, they might share some phenotypic or genetic similarity but the differences among different populations in similar habitats were often, to my eye, as striking as the similarities. A couple of talks near the end of the meeting brought this to the idea to the front of my brain and thus precipitated this post. First, Joop Ouborg showed that the genetic basis for inbreeding depression was almost entirely non-overlapping between different plant species. Second, Freddy Chain showed that lake-stream stickleback divergence in five independent watersheds was almost entirely non-parallel at the genetic level. In short, the fact that evolution is generally non-parallel (or non-convergent) is remarkably parallel (or convergent).

Of course, these are just my interpretations and I have to confess that I have been wrong before – even quite recently. Take grappa, for instance; that crazy Italian drink made by fermenting the leftovers from the pressing of grapes to make wine. Distinctively musty, this drink is quintessentially Italian and is wonderful when drunk for the first time late at night in downtown Napoli surrounded by locals cheering their football team against Barcelona. Or is grappa really that good? Maybe I just liked it because of the context and novelty. Indeed, subsequent consumptions of grappa have further separated the drink from the context and somewhat decreased my enthusiasm. Well, I told the above sad tale at dinner to Nelson Hairson, Luc De Meester, and Isabelle Olivieri right after Nelson ordered grappa. Bah, says Nelson, grappa is good even outside of the context. Ok, then, I challenged him, name three mainstream drinks worse than grappa. And then Isabelle had a brilliant idea – Nelson should pick one drink on the menu that was worse that grappa. That will get him, I figured. So Nelson takes a careful academic look at the menu and pronounces that “Spiriteux de poivre” would be worse. So we ordered this drink and passed it around the other end of the table, where they had not heard our argument and didn’t know what the drinks were: a single-blind experiment if you will. And the verdict: grappa was not very good – but Spiriteux de poivre was infinitely worse.

The Texas gunslinger re-envisioned

Back to parallel evolution. The idea that (even) parallel evolution is often non-parallel was the focus of the meeting that I had in Austin with Dan Bolnick, Yoel Stuart, Dieta Hanson, Rowan Barrett, and Katie Peichel. We had recently received money from the NSF to quantify the non-parallel and parallel contributions to lake-stream stickleback divergence. We will use 16 independent lake-stream pairs to quantify parallelism at the ecological level, the morphological level, and the genetic level. We will then ask to what extent parallelism and non-parallelism at each level can be explained by parallelism and non-parallelism at the other levels. This meeting was set up to plan our first real field season. But, in reality, that was really just the excuse because my main memories involve eating outstanding tacos and barbeque, drinking copious amounts of beverages from Texas, California, and Scotland, and climbing, both in Dan’s backyard “cave” and at Reimer’s Ranch. (If you are at the NSF, I am just kidding.) To push a metaphor perhaps too far, all climbing routes go in an overall parallel direction (up!) but each one follows its own idiosyncratic route and often ends up in a different place.

Parallel?

Multitasking par excellence- or "why McGill hired Dr. Barrett"

Carnival of Evolution #56: World Travel Edition!

  Carnival of Evolution #56 is now posted.  This month’s contribution from eco-evo evo-eco is a great post by Victor Frankel (who also did our featured post last month!) on how the rise of the Isthmus of Panama has affected evolution of the local species.  Check out all the other cool posts at the Carnival for the latest from the evolution blogosphere.

  The theme of this Carnival is world travel.  But why stop with just one planet’s worth of eco-evolutionary dynamics?  In the spirit of Andrew’s recent post asking whether eco-evolutionary dynamics are stronger in the tropics: should we expect eco-evolutionary dynamics to be stronger or weaker on other planets?  Perhaps it depends on how tropical their climates are.  I'll leave you to ponder that, inspired by this astrobiology-themed image (from NASA!).