Evolutionary consequences of indirect trophic interactions

This post is by Philipp Hirsch - I am just putting it up. (Andrew) 

When teaching ecology classes I frequently apply a method called concept-mapping. In concept-mapping assignments students are asked to connect different concepts on a sheet of paper with labeled arrows, thus outlining the interrelations among these concepts. I noticed that, if you wait long enough, every concept will be connected to every other. In addition to initially drawn solid arrows, over time, there are more and more dashed arrows drawn.  Students like to expand the assignment to include dashed arrows that indicate indirect interactions and feedbacks among concepts.

This very much reminds me of food webs. While some arrows e.g. between predator and prey are obvious (quickly drawn) there are a lot of indirect interactions between non-adjacent components in the food web (dashed lines that require a second thought). Such indirect ecological interactions are increasingly recognized as being ubiquitous and ecologically relevant. The question then becomes: What are the evolutionary consequences of indirect trophic interactions?

Lake Erken’s shoreline and all the other lakes in our survey are near-pristine except for the introduction of the zebra mussel (Photo credit: PE Hirsch).

In a recent paper we addressed this topic. We asked how indirect effects of one species that cascade through the food web can contribute to the early stages of adaptive divergence. As a model species we used perch which show a clear phenotypic divergence between littoral and pelagic forms. The magnitude of this divergence is dependent on the availability of profitable habitat-specific resources. Feeding on these resources leads to a specialization of perch morphology to resource-acquisition, mainly through phenotypic plasticity. To study how this phenotypic divergence is affected by indirect interactions we compared perch from lakes in Sweden that were either pristine or invaded by the zebra mussels.

Zebra mussels are numerous in Lake Erken and in the other studied mussel-lakes (Photo credit: PE Hirsch)

Perch do not feed on zebra mussels. Zebra mussels affect both the benthic and pelagic food base of lakes by filtering nutrients from the water column and providing a surplus of structure and nutrients on the bottom. Their filtering activity also increases water clarity. We therefore hypothesized that zebra mussels indirectly increase the phenotypic divergence between littoral and pelagic perch by increasing the habitat-specific food resources for perch.

Indeed we found higher densities of large benthic prey items in the littoral and higher densities of large zooplankton in the pelagic zone of mussel-lakes. Water clarity was also higher in lakes with zebra mussels. Finally, the magnitude of divergence between littoral and pelagic perch was higher in lakes with zebra mussels.

Phenotypic divergence between pelagic (top individuals) and littoral (individuals below) was higher in lakes with zebra mussels (Photo credit: PE Hirsch)

We suspect that indirect interactions between zebra mussels and perch could have triggered this increase in divergence. We considered two main causes of how the mussel-mediated resource changes might indirectly affect perch divergence. First, increases in littoral and pelagic resource density might allow for stronger plastic responses and therefore better adaptation of pelagic and littoral individuals to their different environments. Second, increases in water clarity and resource density might increase disruptive selection acting on morphology -although direct evidence is lacking.

The stronger plastic response in perch from lakes with zebra mussels plausibly results from the surplus of energy-rich invertebrates and zooplankton that specialized phenotypes can exploit in mussel-lakes. A higher growth rate in perch allows for a faster modulation of body shape to better fit the feeding mode. Costs of phenotypic plasticity should also be lower when profitable resources are plenty.

Perch feeding on zebra mussels on the underside of a foot bridge in one of the study lakes (Photo credit: PE Hirsch)

The possible change in disruptive selection regime in mussel-lakes is more complex and partly counter-intuitive. Most studies predict that increasing resources (as seen here in lakes with zebra mussels) should reduce disruptive selection. The puzzling question is how disruptive selection can be more pronounced in lakes with zebra mussels, given the higher resource densities. We propose that the combination of higher water clarity and higher resource density might enhances the connection between diet and morphology. Recently, we could show that if the water is clearer then resource use as well as morphology are more divergent between littoral and pelagic perch (Bartels et al. 2012). The stronger connection between diet and phenotype in mussel-lakes might then affect the selective regime i.e. the “disruptiveness” increases favouring extreme littoral and pelagic phenotypes (with more specialized diet and morphology) and disfavouring intermediate ones. However, at present this remains an educated guess and an exciting field for future research. In any case, on the concept map of the studied lakes the drawing of at least one dashed line between zebra mussels and perch is certainly warranted.

Here’s the link to our paper:

Hirsch P.E.,  Eklöv P.  and Svanbäck R. Indirect trophic interactions with an invasive species affect phenotypic divergence in a top consumer. Oecologia

http://link.springer.com/article/10.1007%2Fs00442-013-2611-1

Capture-recapture or je ne se quoi

When you think of Montpellier there are probably a number of things that readily pop into mind: Mediterranean architecture, deep blue skies, red wine and an astonishing number of sea-food dishes are probably among the first ones. But Montpellier is also renown for being in the forefront of capture-recapture data analysis ­­–well, maybe not Montpellier itself but rather CNRS campus Montpellier, but that really doesn’t matter. It was a workshop on this capture-recapture data analysis the reason of my first trip to the beautiful French Mediterranean.

The workshop "Modelling individual histories with state uncertainty" started with a wine and cheese degustation that served as an icebreaker. Between mingle and mingle I got to know some of the other people that came to the workshop. The group was quite diverse. Most people were working with very charismatic animals like arctic foxes or elephant seals, which made me a bit jealous, yet I always stood very proud saying I worked with guppies. During the first day of the workshop I got to learn the 101 of capture-recapture models: not finding an individual does not mean it is dead. Pretty straight forward if you leave the matrices out. Basically, the probability of different events (capturing or not an individual at time t) is not the same as the probability of different states (being alive or not between time t and t+1), and there will always be some uncertainty around them. Voilà! This can be then easily extrapolated to multiple states and events (being dead or alive in site a, b, c or d; captured in site a, b, c or d, or not captured at all). You can even add some fixed factors here and there, some covariates, and even some heterogeneity. This is what we spent mastering the next few days –or at least trying to– the art of multi-state capture recapture modelling.

In between sessions I managed to enjoy what Montpellier had to offer, this of course with the help of some French tour guides that were also willing to talk about science in more bohemian environments like the local beer shop or with a pique-nique à la française, all with a very Haussmann’s style.

At the end of my week-long trip to Montpellier I understood the power of capture-recapture models with state uncertainty, and how they can be easily applied to answer a wide array of ecological and evolutionary questions. Most importantly, I understood the value of proper tools to analyze long-term data where uncertainty around states can lead to wrong conclusions and hinder relevant biological patterns. So if you have a long term data set with capture-recapture information, I would greatly encourage you to pay a visit to the people in Montpellier, as they have started to hold this workshop on a yearly basis ;)

*I would like to thank QCBS for sponsoring this trip, the organizers Roger Pradel, Rémi Choquet, Olivier Gimenez, Jean-Dominique Lebreton, Gilles Gauthier, Guillaume Souchay and Louise Van Oudenhove. I would also like to thank the very nice people I met in Montpellier, who are too many to write, but here are a few: Pirerre Dupont, Florian Orgeret, Lorelai Guery, Ciara Bertulli, Cecilia Pinto, Catherine Baltazar.

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.

--------------------------------------------------

*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.