More adventures in Speciation

As Andrew’s last post demonstrates, uncovering the primary mechanisms of speciation - barriers to gene exchange between populations - remains a topic of active debate, even among the most eminent researchers in the field. Part of this debate potentially, and perhaps paradoxically, is a result of the fact that the field was dominated by conceptual and theoretical contributions until the last decade which has seen an explosion of empirical research. The main conceptual mechanisms of speciation, measured as the accumulation of reproductive isolation, are rooted in sexual selection, ecological differences (i.e. natural selection) and physical isolation. Data from different systems often fit nicely into one of these three umbrellas, lending support to the original theories, but leave us scratching our heads to understand which mechanism(s) are THE main drivers of the process. Our latest paper,recently published in PLoS ONE (http://dx.plos.org/10.1371/journal.pone.0015659) suggests that rather than looking for a single winner, the answer may become clearer by closer integration. In collaboration with researchers from the University of Maine and Dalhousie University, we examined patterns of female mate choice and male mating success in Trinidadian guppies from nine populations in 4 different rivers.

Avid readers of this blog or anyone who has picked up a biology textbook, will be familiar with the guppies, as they are one of the few model organisms for studying adaptation in the wild. The guppy’s small size, agility, and freakishly high fecundity allowed it to colonize upstream sections of rivers above large waterfalls, unlike its larger, predatory neighbours. This sets the stage for a natural laboratory for observation and experimentation as upstream guppies have escaped to guppy heaven, banishing their cousins to the hell of a life of high mortality risks. But of course, what doesn’t kill you makes you stronger, and high-predation guppies have indeed adapted to their lives in hell allowing them to escape quickly, mature early, hide well, and limit their sexual colouration to remain as inconspicuous as possible. Their cousins above are not so careful or visually discreet. Males in particular are generally more colourful, possibly because females generally prefer to mate with colourful males. When these guys move or get flushed downstream, we know they suffer the consequences with reduced survival.

Since ecological and physical isolation has led to adaptive differences in multiple traits, one of which is a target of both mate choice and survival, the stage is set for speciation as far as has been documented in similar systems. Yet, evidence for reproductive isolation between guppy populations has so far been sparse and inconsistent. What we found is that while low-predation females consistently discriminate against high-predation males (regardless of their river of origin), high-predation females only discriminate against low-predation males from upstream in their own rivers. This pattern is not only consistent in lab tests from paired populations in three different rivers, but also evident in the field experiments. Here, we set up enclosures in a high-predation stream and allowed resident males and two populations of low-predation males (one neighbour population and another further away) to compete for fertilizations with resident virgin females. Paternity analyses revealed that high-predation males only substantially outcompete the neighbouring low-predation males. Together, this study shows evidence for mating isolation in guppies but this isolation is likely driven by more than one mechanism: for females in high-predation environments, it’s selection against maladapted low-predation migrant males (reinforcement), whereas for low-predation females it’s selection against particular traits related to survival in high-predation. What these traits are specifically, how they influence mating success, and how preferences are evolving and respond to selection remain open questions and important areas for future research.

So although the latest chapter in the guppy story doesn’t necessarily fall into textbook expectations, it nonetheless shows the strength in not only looking for evidence of speciation where it’s most likely to be found, but by focusing on situations where it isn’t apparent we may be able to start to untangle the ecological limits to evolutionary differentiation and the evolutionary limits to ecological differentiation.

Magic and muggle in Austria speciation meeting

Set against a backdrop of vineyards and castles, and held in the summer palace of the Hapsburgs in Laxenburg, was the First European Conference on Speciation Research, organized by Ulf Dieckmann and Ake Brannstrom. Thirty or so talks and many posters fomented a great environment for argument and debate – with or without liquid encouragement.

A principle item of argument was the role of “magic traits” in speciation. The term was originally coined by Sergey Gavrilets in a derisive way to suggest the implausibility of natural populations having traits (or genes) that were under divergent natural selection and also influenced mate choice. Traits/genes like this make speciation, particularly sympatric speciation, much easier and frequently appear in theoretical models demonstrating that sympatric speciation is “plausible.” The funny thing was that empiricists quickly pointed to a large number of traits that seemingly do have these joint effects, including body size in stickleback, beak size in finches, color in butterflies and hamlet fishes, and habitat choice in herbivorous insects. And so magic traits quickly became a rallying point for people studying speciation in sympatry or parapatry: i.e., speciation with gene flow. Now many empirical studies invoke the existence of apparent magic traits in their study system as a way of suggesting an easy, perhaps even inevitable route to speciation. And new theoretical models are now invoking magic traits in a proactive way, rather than cloaking them in alternative genetic structures and explained them away in an apologetic fashion.

So what’s to debate? The first point was that some people felt the term shouldn’t be invoked because it implied that such traits are not believable – when they may actually be common. Others at the meeting disliked the term because it wasn’t defined precisely – although several people are working on doing precisely this. My own point of concern was partly related to this ambiguity. In particular, just how much of the reproductive isolation evolving between two species must such a dual-effect trait explain to warrant the term “magic.” To me, magic implied something important - perhaps speciation wouldn’t have occurred without the magic trait. But it was pointed out by Maria Servedio that the original definition doesn’t imply any effect size. I resisted this for some time, but then realized that not all magic has to be important. Hermione might use “trivial magic” to make a feather float, whereas she might use “important magic” to save Harry’s life. Both actions are magic but only the latter matters. So maybe we need to distinguish “trivial magic traits” from “important magic traits.” Best of all, however, Eva Kisdi noted that the appropriate antonym for a non-magic trait is clearly a “muggle trait,” and so I realized I loved the term.

And so I stayed out until 2 am drinking and arguing with Maria Servedio, Dan Bolnick, Louis Bernatchez, and Isabelle Olivieri. Then I caught a cab for the airport at 4:30 am, and watched the magic of lightly falling snow illuminated by the light from ancient buildings against the inky backdrop of the pre-dawn sky. Trivial perhaps – but no less magic to a muggle.

Other blog posts about the conference:

http://benaustria.blogspot.com/2010/12/speciation-2010.html

http://svenssonresearchlaboratory.blogspot.com/2010/12/greetings-from-speciation-meeting-in.html

Anthropogenic disturbance and evolutionary parameters from a natural population of lemon sharks

Little is known about the potential for adaptive evolution to save natural populations faced with environmental change, despite an increasingly present human hand in modifying their environment. These modifications likely reduce the degree to which populations are adapted to their local conditions, thereby decreasing mean fitness and possibly leading to local extinction. Such adaptive processes depend on several factors such as population connectivity, initial population size, mortality rates, adaptive plasticity (or maternal effects), genetic variation, and the strength and form of selection. And yet few studies to date assess if and how each of these factors has changed in the face of anthropogenic forces.

A recent paper from the Hendry lab attempted to fill this gap by combining long-term monitoring (13 years) of marked lemon sharks (Negaprion brevirostris) at an isolated nursery lagoon (Bimini, Bahamas) with genetic pedigree reconstruction (DiBattista et al. 2011, Evolutionary Applications 4[1]: 1-17). DiBattista et al. (2011) assessed whether habitat loss influenced population size, juvenile mortality, maternal effects, genetic variation, and selection in this lemon shark population. This analysis was only possible because recent human activities (i.e., mangrove removal) associated with a large-scale development project at Bimini conveniently bisected their dataset. Contrary to expectation, they found that samples after the disturbance (relative to before the disturbance) showed an increase in 1) the number of sharks breeding at this site, 2) neutral genetic variation, and 3) additive genetic variation for several key juvenile life-history traits (i.e., body size and growth). They also found a dramatic change in selection acting on those same life-history traits; habitat loss here appears to have changed which phenotypes are now favored by natural selection.

The authors therefore conclude that some species may be tolerant to some habitat loss, although this likely depends on the length and duration of the disturbance. Similarly, high levels of gene flow among population may act to buffer losses in neutral and additive genetic variation, and in some cases increase it. Based on the observed changes in the strength and sometimes direction of natural selection acting on life-history traits in this population, it would seem that habitat loss may impede adaptive processes by altering the fitness landscape.

Joseph DiBattista (NSERC postdoctoral fellow at the Hawaii Institute of Marine Biology, University of Hawaii)

Photo Credit

DiBattista JD, Feldheim KA, Garant D, Gruber SH, and Hendry AP (2011). Anthropogenic disturbance and evolutionary parameters: A lemon shark population experiencing habitat loss. Evolutionary Applications 4(1): 1-17.

(http://onlinelibrary.wiley.com/doi/10.1111/eva.2010.4.issue-1/issuetoc)

Photo Credit: Matthew Potenski (http://www.matthewpotenskiphoto.com/)

*Save one, none of the other authors were bitten, maimed, or otherwise harmed during the tagging of said lemon sharks.

Evolutionary causes and consequences of plasticity

Changes in phenotype directly induced by the environment, called phenotypic plasticity, can have strong evolutionary consequences. Recent papers from the Hendry lab have examined plasticity-evolution relationships (Crispo et al., 2010, EER 12: 47-66; Thibert-Plante & Hendry, in press, JEB).

Crispo et al. conducted a meta-analysis to determine whether phenotypic plasticity generally tends to evolve as a response to human-induced changes to the environment. They examined 20 studies in which plasticity was estimated between populations that were under the influence of anthropogenic stressors, and between closely related populations that had not. They found that it many cases, plasticity had evolved in response to anthropogenic disturbance, when compared to their non-disturbed counterparts. The direction of this change, however, varied greatly among taxa and trait types. For example, invertebrates often showed the evolution of increased plasticity in life history traits and decreased plasticity in morphology, whereas plants showed no trends in plasticity evolution. The authors therefore conclude that plasticity and its evolution might be important for adaptation, but that it should be examined on a case-by-case basis, rather than making general statements about whether increased or decreased plasticity is likely to evolve as an adaptive strategy. The full article can be found at http://www.evolutionary-ecology.com/abstracts/v12/n01/ffar2517.pdf.

Thibert-Plante and Hendry looked at the consequences of phenotypic plasticity on ecological speciation. The consequences of plasticity for ecological speciation depend on the timing of dispersal relative to the expression of the plasticity. On the one hand, if plasticity is expressed early in development, before any dispersal, the individuals dispersing to a different environment will have reduced fitness, relative to the case of no plasticity. On the other hand, if plasticity is expressed after dispersal, the fitness cost of dispersing can be greatly reduced or even completely removed. Those facts are of great importance in the context of ecological speciation, where we study the rise and fall of barriers to gene flow among populations. More details can be found at http://onlinelibrary.wiley.com/doi/10.1111/j.1420-9101.2010.02169.x/abstract.

Xavier Thibert-Plante (FQRNT and NIMBioS postdoctoral fellow, Knoxville)

Erika Crispo (NSERC postdoctoral fellow in Royal Ontario Museum, Toronto)

* The authors have no competing interest, apart from space in high profile scientific journals.

Constraints on ecological speciation?

“Constraints on speciation suggested by comparing lake-stream stickleback divergence across two continents” – just appeared in Molecular Ecology (19:4963-4978). This paper tests whether the striking phenotypic (foraging morphology) and neutral genetic (microsatellite) divergence that characterizes incipient speciation across lake-stream transitions in Canadian (Vancouver Island) stickleback fish can also be found in some very young (150 years or less) European lake-stream pairs. The main findings are that, first, morphological divergence is generally much lower in the European population pairs, and there are striking overall phenotypic differences between the continents. Although alternative explanations are possible, it seems likely that there are some genetic constraints. Alleles that serve in adaptive lake-stream divergence (e.g. in body shape) in Canada appear to be absent in Europe. Limited time for morphological adaptation might also play a role. Second, there is only trivial divergence in microsatellite frequencies in the European pairs, contrary to the very high divergence found in some Canadian watersheds. This result suggests high gene flow and no evolved reproductive barriers in the young European systems. However, individual-based simulations tailored to these systems reveal that, even if reproductive barriers were absolute, it would be unlikely to see them with neutral markers. Those markers just evolve too slowly. It is thus possible that despite weak morphological divergence, reproductive isolation in Europe pairs could be strong, and hence we are simply dealing with the earliest stages of speciation. This could be possible if isolation is mediated by other traits not studied (e.g. behavior). Follow-up work is examining genome-wide divergence in these lake-stream pairs. This post was contributed by Daniel Berner.

Stickleback porn generates duelling papers

Mating isolation is a frequent contributor to ecological speciation – but how consistently does it evolve as a result of divergent selection? An excellent model system to address this question is the threespine stickleback, with its species pairs that evolved multiple times in a diversity of contrasting habitats. Mating isolation could arise through assortative mate choice, such as when females actively choose a male of their own type or when male-male competition does the job for them.

We designed an experiment aiming to demonstrate that at least one of these possibilities would lead to mating isolation in­ the Misty watershed on Vancouver Island, British Columbia. This watershed contains a very divergent but interconnected pair of lake-inlet stream stickleback. In the laboratory, gravid females were introduced into a tank where they could choose between, and be competed for, by two males of different types: lake, stream, or hybrid. Despite very different courtship behaviours of lake and stream males, and seemingly inferior levels of competition of hybrid males, mating patterns were not assortative. In fact, hybrid males obtained the most females. It is hard to define stickleback attractiveness if you are not a stickleback yourself, but hybrid males were reasonably large and aggressive (unlike stream males) and showed some elegance in their courtship (unlike lake males). This combination may have promoted their high mating success.

These results stand in contrast to other stickleback pairs which do show assortative mating, such as the benthic-limnetic and anadromous-freshwater pairs. So far, other studies in the Misty system also haven't found strong reproductive barriers. This is either because we haven't been looking close enough to find the real ecological cause(s) of reproductive isolation, because the real cause(s) are not visible in standard laboratory experiments, or because there is no strong progress towards ecological speciation. Either way, our results highlight the importance of considering the various factors that promote or constrain progress toward ecological speciation.

And just when we were checking the online version of our paper, a very similar study appeared online. Christophe Eizaguirre and colleagues from the Max-Planck Institute for Evolutionary Biology (Plön, Germany) showed that in their lake and stream system, stickleback do choose assortatively based on olfactory cues in a flow channel. Previous studies at MPI Plön have shown that lake and stream stickleback are infected by different parasite communities, and are highly divergent for MHC, a set of immune genes. Interestingly, these genes are also involved in mate choice. Being under both natural and sexual selection, MHC has the potential to act as a “magic trait”, accelerating ecological speciation.

The standing contrast then is that Plön stickleback choose their own type (lake or stream) based on olfactory cues, whereas Misty stickleback don't choose their own type (lake or stream) based on olfactory cues and visible cues together. The latter situation is certainly a more realistic setting. However, another contrast between our experiments was that Misty stickleback were second generation lab-reared fish, while Plön stickleback were captured in the wild. This is important as mating preferences could be learned based on imprinting on conspecifics or experience with heterospecifics (Kozak et al. 2009; Behav. Ecol). Much more work needs to be done to assess the consistency of mating barriers in stickleback, perhaps through reciprocal experiments: what if Misty sticklebacks can only smell their potential mates, and what if Plön sticklebacks can actually see their potential mates? To be continued...

Greetings from Belgium,

Joost Raeymaekers

Raeymaekers JAM, Boisjoly M, Delaire L, Berner D, Räsänen K & Hendry AP (Early online). Testing for mating isolation between ecotypes: laboratory experiments with lake, stream and hybrid stickleback. Journal of Evolutionary Biology. (http://onlinelibrary.wiley.com/doi/10.1111/j.1420-9101.2010.02133.x/abstract)

Eizaguirre C., Lenz T.L., Sommerfeld R.D., Harrod C., Kalbe M. and Milinski M. (Early online). Parasite diversity, patterns of MHC II variation and olfactory based mate choice in diverging three-spined stickleback ecotypes. Evolutionary Ecology. (http://www.springerlink.com/content/0269-7653/?k=10.1007%2fs10682-010-9424-z)

Alewife feeding leads to feedbacks

The concept of eco-evolutionary feedbacks unites two well-established theories, which have traditionally existed in isolation. The theory of adaptive radiation, which comes from evolutionary biology, posits that the biotic and abiotic environment determines niche availability, and that lineages diversify until available niches are filled. In contrast, theories of environmental modification, which come from ecology, posit that the activities of organisms modify important aspects of the biotic and abiotic environment. The concept of eco-evolutionary feedbacks integrates these perspectives by recognizing that both processes can occur simultaneously. According to this integrated theoretical framework, adaptive diversification can simultaneously shape and be shaped by the niche-modifying abilities of organisms.

Compelling evidence for the importance of eco-evolutionary feedbacks in the wild comes from our work on alewife-zooplankton interactions in lakes. Anadromous alewives (Alosa pseudoharengus) migrate annually from the Atlantic Ocean to inland lakes where they spawn. Juveniles rear in these lakes, usually for one summer, before departing for the ocean to mature. Our research shows that the isolation of lakes from the ocean by human-constructed dams has led to the evolution of landlocked alewife populations. The ecological effects of landlocked alewife populations are well known from classic work in Connecticut lakes by John Brooks and Stanley Dodson and from studies of the alewife invasion of the Great Lakes. Predation by landlocked alewives drives dramatic shifts in mean body size, biomass, and species composition of crustacean zooplankton. But what about anadromous alewives? Our work shows that the ecological effects of anadromous alewives differ markedly from those of landlocked alewives. In lakes harboring anadromous populations, zooplankton effects are largely seasonal – when the juveniles depart each fall, large-bodied zooplankton recover. However, in landlocked lakes predation pressure is year-round – zooplankton communities are continuously dominated by small-bodied species. A key question is: how do landlocked alewives persist under such unfavorable (small-bodied) prey conditions? Our research shows that the answer lies in contemporary evolution. After eliminating large zooplankton from the lake, landlocked alewife populations rapidly evolve morphological traits (gape width and gill raker spacing) and behavioral traits (prey selectivity) that enable them to be efficient foragers on small-bodied zooplankton. Altered foraging traits then further modify zooplankton community structure and influenced the strength of trophic cascades.

The above results point to an eco-evolutionary feedback. The contemporary evolution of landlocked alewife populations from anadromous ancestors led to changes in zooplankton communities, which in turn shaped the evolution of alewife foraging traits, with then further impacts the structure of prey communities and cascading trophic interactions. Thus, rather than adapting to an existing ecological template (niche), which would be the assumption based on traditional theory, alewives participate in creating the niche to which they are adapted. And the resulting phenotypic divergence then drives further ecological effects. Not a bad days work for a hungry little fish.