Novel habitat, predictable responses: niche breadth evolution in geckos

At a time of immense ecological change (such as the Anthropocene), organisms have a few options. They can move, tolerate, adapt, or, in failing to do so, face extinction. One or most of those options may not be available to most species. For example, the question of whether most species can adapt rapidly enough to maintain populations in degrading habitats, rising temperatures and increasing environmental variability has (at least in part) motivated the study of rapid or contemporary evolution. Studying the probability of successful selection and adaptation over ecological timescales may be very important for understanding the options available to species.

de Amorim et al. (2017, PNAS) describe one such example, where the result of novel environmental change provides a unique opportunity to observe rapid evolution. Beginning in 1996, a reservoir in Central Brazil was created by flooding a huge area, creating nearly 300 islands and massively affecting local wildlife. Gymnodactylus amarali was the most common lizard (a termite-specialized gecko), and the authors sought to determine the impacts of rapid isolation on the species.

Isolation on islands created an new set of biotic conditions – other termite eating lizards went extinct on islands, increasing the available diet breadth, particularly increasing the availability of larger termites. Larger termites require geckos have the physical ability to catch and processes them. One possibility is that to take advantage of this new resource, G. amarali on islands would need larger heads. Because larger heads and bodies come with increased energy requirements, the authors predicted that the island geckos would have larger heads, but no change in overall body size.

Termite size increased on average on islands; for the same body size, head length tended to be larger on islands. 

Indeed, island geckos had higher diet breadths, driven by the availability of larger termites and an increased ability to catch them via larger head lengths. Increased diet breadth was accompanied by increased head size, but not body size.

Notably, this change in diet and associated characters occurred independently across multiple reservoir islands, beginning once they were isolated from the mainland. This is an interesting example of rapid evolution precisely because evolution took the same path in every case, and because it occurred so rapidly (less than 15 years). This is not always the expectation - in many cases, human activities (e.g. fragmentation) will increase decrease population sizes and genetic diversity, thereby increasing drift and decreasing the predictability (and speed) and adaptation. Contrasts between successful and unsuccessful adaptive responses will help us understand better how and when fragmentation threatens populations.

Mariana Eloy de Amorim, Thomas W. Schoener, Guilherme Ramalho Chagas Cataldi Santoro, Anna Carolina Ramalho Lins, Jonah Piovia-Scott, and Reuber Albuquerque Brandão. 2017. Lizards on newly created islands independently and rapidly adapt in morphology and diet. PNAS. 114 (33) 8812-8816.

Experimental macroevolution at microscales

Sometimes I find myself defending the value of microcosms and model organisms for ecological research. Research systems do not always have to involve a perfect mimicry of nature to provide useful information. A new paper in Evolution is a great example of how microcosms provide information that may not be accessible in any other system, making them a valuable tool in ecological research.

For example, macroevolutionary hypotheses are generally only testable using observational data. They suffer from the obvious problem that they generally relate to processes of speciation and extinction that occurred millions of years ago. The exception is the case of short generation, fast evolving microcosms, in which experimental macroevolution is actually possible. Which makes them really cool :-) In a new paper, Jiaqui Tan, Xian Yang and Lin Jiang showing that “Species ecological similarity modulates the importance of colonization history for adaptive radiation”. The question of how ecological factors such as competition and predation impact evolutionary processes such as the rapid diversification of a lineage (adaptive radiation) is an important one, but generally difficult to address (Nuismer & Harmon, 2015; Gillespie, 2004). Species that arrive to a new site will experience particular abiotic and biotic conditions that in turn may alter the likelihood that adaptive radiation will occur. Potentially, arriving early—before competitors are present—could maximize opportunities for usage of niche space and so allow adaptive radiation. Arriving later, once competitors are established, might suppress adaptive radiation.

More realistically, arrival order will interact with resident composition, and so the effects of arriving earlier or later are modified by the identities of the other species present in a site. After all, competitors may use similar resources, and compete less, or have greater resource usage and so compete more. Although hypotheses regarding adaptive radiation are often phrased in terms of a vague ‘niche space’, they might better be phrased in terms of niche differences and fitness differences. Under such a framework, simply having species present or not present at a site does not provide information about the amount of niche overlap. Using coexistence theory, Tan et al. produced a set of hypotheses predicting when adaptive radiation should be expected, given the biotic composition of the site (Figure below). In particular, they predicted that colonization history (order of arrival) would be less important in cases where species present interacted very little. Equally, when species had large fitness differences, they predicted that one species would suppress the other, and the order in which they arrived would be immaterial. ­

From Tan et al. 2017

The authors tested this using a bacterial microcosm with 6 bacterial competitors and a focal species – Pseudomonas fluorescens SBW25. SBW25 is known for its rapid evolution, which can produce genetically distinct phenotypes. Microcosm patches contained 2 species, SBW25 and one competitor species, and their order of arrival was varied. After 12 days, the phenotypic richness of SBW25 was measured in all replicates.

From Tan et al. 2017. Competitor order of arrival in general altered the final phenotypic richness of SBW25.

Both order of arrival and the identity of the competitor did indeed matter as predictors of final phenotypic richness (i.e. adaptive radiation) of SBW25. Further, these two variables interacted to significantly. Arrival order was most important when the 2 species were strong competitors (similar niche and fitness differences), in which case late arrival of SBW25 suppressed its radiation. On the other hand, when species interact weakly, arrival order had little affect on radiation. The effect of different interactions were not entirely simple, but particularly interesting to me was that fitness differences, rather than niche differences, often had important effects (see Figure below). The move away from considering the adaptive radiation hypothesis in terms of niche space, and restating it more precisely, here allowed important insights into the underlying mechanisms. Especially as researchers are developing more complex models of macroevolution, which incorporate factors such as evolution, having this kind of data available to inform them is really important.

Interaction between final phenotype richness and arrival order for B) niche differences and D) fitness differences. S-C refers to arrival of SWB25 first, C-S refers to its later arrival. 

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

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

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

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

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

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

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

NSF funds Project Baseline

NSF approved 1.2 million dollars for a unique and visionary idea: collect 12 million seeds and store them in seed banks for years to come. And while storing seeds for the future doesn't sounds so different from what other groups have already done, where Project Baseline differs is that this seed bank is not only a conservation measure--preserving natural genetic variation from plant populations for the future--but also an opportunity to track the effects of changing climate on the direction and rate of evolution in these species.

This idea was first explored in "The Resurrection Initiative: Storing Ancestral Genotypes to Capture Evolution in Action" (Franks et al 2007). By collecting and storing seeds from both within and across populations throughout the range of a species, ancestral and descendent populations can be compared in the not too distant future. The role of adaptive evolution and range shifts can be explored through this lens. Project Baseline is a great example of how much we can learn from long-term, collaborative experiments and projects (other examples include NutNet , NCEAS), and how valuable funding such projects should be considered.

Adaptation and dispersal = (mal)adapted

Ever since Darwin, we often think of organisms as being in a constant battle against other organisms and local environments. Thus natural selection and the resulting arms race results in organisms highly adapted to local conditions and against local antagonists. At the same time, and especially driven by theoretical advances in the 1990's, researchers began to ask how dispersal -that is, the flow of genetic material from elsewhere, can disrupt local adaptation. On the one hand it may provide genetic variation allowing for novel solutions to new difficulties. On the other hand, dispersal may reduce the prevalence of fitness-increasing genes within local populations.

In a simple but elegant experiment, Jill Anderson and Monica Geber performed a reciprocal transplant experiment, moving Elliott's Blueberry plants between two habitats. One population was from highland, dryer habitats and the other from moist lowlands. They further evaluated performance in greenhouse conditions. Their results, published in Evolution, show that these two populations have not specialized to local conditions. Rather, due to asymmetric gene transfer, lowland individuals actually performed better when planted in highlands than compared to their home habitat. Further, in the greenhouse trials, lowland species did not perform better under higher moisture conditions. While genetic or physiological constraints may also limit adaptation, Anderson and Geber present a fairly convincing case that gene flow is the culprit.

These results reveal that populations may actually be relatively mal-adapted to local conditions, which has numerous consequences. For example, we need to be cognizant of adaptations to particular conditions when selecting populations for use in habitat restoration and when trying to predict response to altered climatic or land-use conditions. Importantly what does this mean for multi-species coexistence? Dispersal seems to limit the ability to adapt, and thus, better use local resources or maximize fitness, making for a better competitor. At the same time, dispersal can offset high death rates, allowing for the persistence of a population that would otherwise go extinct. Understanding how these two consequences of dispersal shape populations and communities is an interesting question, and work like Anderson and Geber's provides a foundation for future studies.

Anderson, J., & Geber, M. (2009). DEMOGRAPHIC SOURCE-SINK DYNAMICS RESTRICT LOCAL ADAPTATION IN ELLIOTT'S BLUEBERRY (

)
Evolution DOI: 10.1111/j.1558-5646.2009.00825.x