Wednesday, July 22, 2015

Habitat preference and speciation



Back in 2006, during my field work on Vancouver Island for my postdoc project with Andrew Hendry on threespine stickleback in contiguous lake and stream habitats, I was deeply impressed by the phenotypic differentiation these populations exhibit across extremely steep ecological transitions – often without any obvious physical dispersal barrier. For example, the left picture below shows the abrupt transition from Robert’s Lake (background) into its outlet stream (foreground). Morphological divergence between these populations was immediately obvious in the field (right picture: adult stream male on top, adult lake male below), and analyzing microsatellite data later showed that phenotypic divergence was paralleled by equally striking genetic shifts (for details see Berner et al. 2009, Evolution). This made me really think about what reproductive barrier(s) could maintain such steep divergence in the face of dispersal opportunities, and my intuition was that perhaps lake and stream fish simply wanted to stay in their native habitats, rather than disperse.


In the same period and in the same study region, Dan Bolnick and his crew performed a very cool field experiment: they sampled stickleback from a lake and its inlet stream, marked the sampled fish according to the habitat in which they had been found, released them in the habitat transition, and checked where they then dispersed by re-capture. Put simply, this experiment made clear that each population preferred to return into its original habitat (Bolnick et al. 2009, Evolution).

Inspired by these observations, I felt that theory was needed to explore how habitat preference can promote adaptive divergence and speciation. Of course, a great deal of theory was already available demonstrating that many forms of non-random dispersal can promote divergence, but this evidence seemed rather scattered and often disconnected from biologically realistic contexts. Hence I started a large-scale simulation project with Xavier Thibert-Plante, a theoretician and friend I got to know in Montreal during my postdoc with Andrew. This work was initially tailored to parapatric lake-stream stickleback, but then we abandoned that specific context in favor of a broader study. Our simulation study considers the scenario in which two populations diverge in the face of gene flow, allowing for the simultaneous evolution of ecological adaptation and dispersal modification. This dispersal modification is modeled to arise from several different habitat preference mechanisms, including habitat imprinting during the juvenile stage, phenotype-dependent habitat preference, or a genetically hard-wired preference for a certain habitat type. We felt that this diversity in the mechanisms underlying habitat preference was crucial, because in natural systems where habitat preference has been inferred, the proximate cause of habitat preference is often not clear.


We find that habitat preference will often evolve so as to reduce gene flow between the habitats. This works best and promotes adaptive divergence most effectively when gene flow between the populations is initially substantial – a domain where migration–selection balance under random dispersal permits weak divergence only. This makes habitat preference a particularly relevant factor in the early stages of speciation when other reproductive barriers are still weak or absent. Comparing the different habitat preference mechanisms further reveals that speciation is strongly facilitated by habitat imprinting, whereas mechanisms like direct genetic preference or pure density-dependence are ineffective contributors to divergence. Moreover, we find that divergence with habitat preference is influenced by asymmetry in the size of the diverging populations, and by variation in the number of genetic factors encoding the simulated traits. Overall, our study indicates that habitat preference deserves much wider recognition when studying the divergence and reproductive isolation of populations. If interested, see Berner & Thibert-Plante 2015, J. Evol. Biol. in press. http://onlinelibrary.wiley.com/doi/10.1111/jeb.12683/abstract



 


The figure above is taken from the paper and shows the evolution of habitat preference via an imprinting trait (upper row), and the facilitation of adaptive divergence by this mechanism relative to random dispersal (bottom row), across combinations of the strength of divergent selection and initial dispersal.  (Click image to see at larger size.)

Saturday, July 11, 2015

Phenotype-genotype-fitness maps and genetic bridges between populations

[ This post is by Aaron Comeault; I am just putting it up.  –B. ]

Since Darwin, we have come a long way in refining our knowledge of selection as a driver of evolutionary change. To give just a few examples, we now know that selection exists as different ‘types’ (e.g. divergent, disruptive, or negative frequency-dependent), and can change in its form and strength through space and time. It is also becoming apparent that selection is constantly acting on the genome and therefore influences patterns of molecular variation. These examples help illustrate how our understanding of selection has developed over the last 150 years. However, there is still a great deal to learn.

Recently, access to genetic data has become easier due to new sequencing technologies and methods of genome manipulation. As such, determining the genetic basis of traits is now more feasible, for a wider range of organisms, than ever before. This is a significant advance for evolutionary biologists because knowledge of the genetic basis of traits allow us to forge explicit links between evolutionary processes such as natural selection and the evolutionary response to selection (Gratten et al. 2008; Johnston et al. 2013). An important goal in modern evolutionary biology is therefore to quantify how phenotype, genotype, and fitness interact to influence evolutionary trajectories (i.e. to quantify ‘phenotype-genotype-fitness [PGF] maps’) (Barrett and Hoekstra 2011; Bierne et al. 2011). The Californian stick insect Timema cristinae provides an opportunity to quantify a PGF map because their evolutionary ecology is fairly well known and genomic resources for them are emerging.

These flightless insects can be found on two common plants in the chaparral of coastal California near Santa Barbara: Ceanothus spinosus and Adenostoma fasciculatum. In populations found on C. spinosus the majority of individuals have solid green colouration, but when found on A. fasciculatum, individuals are usually green with a conspicuous white stripe down their back (see image for examples). This dorsal ‘stripe’ is under strong divergent selection between host plants (Nosil and Crespi 2006). Despite the evidence for strong divergent selection acting on the green and green-striped phenotypes, maladaptive (i.e. mismatched with respect to host plant) phenotypes can be found at varying frequencies within any given population (i.e., green individuals on A. fasciculatum and green-striped individuals on C. spinosus). In part, this maladaptive variation is maintained by ongoing gene flow between populations (Sandoval 1994b; Nosil 2009; also see this EcoEvoEvoEco post by Tim Farkas regarding the ecological effects of maladaptive gene flow in T. cristinae). This begs the question: in T. cristinae, what processes maintain gene flow among populations, and maladaptive phenotypic variation within populations, despite strong divergent selection acting on color pattern? Enter the “dark morph” of the T. cristinae system…


Pattern and colour phenotypes of Timema cristinae (click to see at larger size)

In addition to the green phenotypes mentioned above, a “dark morph” that has previously been referred to as “red” or “grey” (Sandoval 1994a) is found at modest frequencies (~10 %) in most populations of T. cristinae. We here refer to this phenotype as “melanistic” (see image above). At that moment during everyone’s PhD studies when they say to themselves, “what the heck is my thesis going to be about?”, Patrik and I discussed focusing on understanding the evolutionary forces working to maintain this enigmatic melanistic phenotype of T. cristinae. At that time we knew little about the ecological / selective factors maintaining the melanistic phenotype; fleshing that out, particularly when added to our growing knowledge of the genetic basis of the colour and colour-pattern phenotypes, could lead to a better understanding of ecological speciation in the T. cristinae system. In a recent paper (Comeault et al. 2015) we present the work that emerged from this. The paper shows how selection acting within populations of T. cristinae can maintain the melanistic phenotype; it also suggests that the melanistic phenotype maintains gene flow among populations, thus acting as a ‘genetic bridge’ that constrains adaptive differentiation and speciation. Below we summarize the diverse data we collected.


A graphical abstract of Comeault et al. 2015 (click to see at larger size)

We first used ecological measurements to provide evidence that melanistic T. cristinae are maintained by factors including resistance to fungal infections, a mating advantage, and increased crypsis on the stems of both host species. We also found evidence that melanistic T. cristinae may disperse between host plants more than green T. cristinae. These results indicated to us that selection acting on the melanistic phenotype is different than that acting on the green and green-striped phenotypes: a multifarious balance of selective agents maintains the melanistic phenotype within both host plant species, whereas green and green-striped individuals are under divergent selection between the two hosts. We now had an idea of the ‘phenotype’ and ‘fitness’ components of the PGF map for colour and colour-patterning in T. cristinae. We next set off to quantify the genetic basis of these traits. This can be an important step in understanding the evolutionary consequences of phenotypic variation because the response to selection is influenced by aspects of the genetic architecture of traits, such as dominance relationships among alleles, epistasis, and the number of loci underlying phenotypic variation.

Using a combination of classical genetic crosses and multilocus genome-wide association mapping, we identified aspects of the genetic architecture of colour patterning and colour in T. cristinae. Results from these analyses revealed the following: (1) different loci control pattern versus color, (2) both traits are under ‘simple’ genetic control with a single locus for each trait controlling the vast majority of phenotypic variation, (3) green colour alleles are dominant to melanistic alleles, and within green individuals the green allele is dominant to the green-striped allele, and (4) both traits map to the same linkage group (i.e., the loci controlling pattern and color are physically linked).

With all three components of the PGF map now in hand, we developed the hypothesis that melanistic T. cristinae act as a ‘genetic bridge’ among populations. Our logic was as follows: if melanistic individuals are not under divergent selection between host plants, they may be free to move between plants and thus facilitate gene flow between them. In addition to simply moving between environments, they would be capable of shuttling locally maladaptive alleles between host plants – because, crucially, green patterning alleles (striped or unstriped) are not expressed in melanistic individuals. To test this hypothesis, our modeling wizard Sam Flaxman helped us develop a tailor-fit individual-based simulation program.

Simulations enabled us to test the relative importance of individual aspects of the melanistic phenotype (such as a mating advantage for melanistic individuals) in facilitating gene flow between host plants. Indeed, the simulations found that the presence of melanistic T. cristinae reduced adaptive differentiation between populations on different hosts and increased rates of inter-host mating (see figure below). These results show how the melanistic phenotype acts as an ‘anti-speciation’ phenotype, mitigating the effects of divergent selection acting on the stripe phenotype. Moreover, we found that these results were robust to removing individual factors attributed to the melanistic phenotype, such as their mating advantage or their propensity to disperse. The one factor that, when removed from the model, did reduce the ‘anti-speciation’ effect of melanistic individuals was the genetic architecture of the colour and pattern traits: when we removed dominance relationships among alleles at the colour and colour-pattern loci, we found that melanistic individuals did not promote maladaptive gene flow or increase levels of inter-host mating. These simulations therefore used the PGF map to empirically quantify an example of an ‘anti-speciation’ phenotype. Our results also highlight how a combined understanding of both the evolutionary ecology and the genetic architecture of phenotypic variation can help us better understand the evolutionary process. We hope that future work in other taxa will continue to illuminate how phenotypes, their underlying genetic architecture, and fitness relationships interact – not only to drive adaptive evolution, but also to constrain it.



Evolutionary effects of the melanistic phenotype. The presence of melanistic individuals within simulated populations reduced adaptive differentiation (Fst) at the locus controlling pattern phenotypes (A), had a slight effect on levels of neutral genomic differentiation (B), and increased levels of inter-host mating (IHM) (C).  (Click to see at larger size).

Works cited

Barrett, R. D. H., and H. E. Hoekstra. 2011. Molecular spandrels: tests of adaptation at the genetic level. Nat. Rev. Genet. 12:767–780. Nature Publishing Group.

Bierne, N., J. Welch, E. Loire, F. Bonhomme, and P. David. 2011. The coupling hypothesis: why genome scans may fail to map local adaptation genes. Mol. Ecol. 20:2044–72.

Comeault, A. A., S. M. Flaxman, R. Riesch, C. Emma, V. Soria-Carrasco, Z. Gompert, T. E. Farkas, M. Muschick, T. L. Parchman, J. Slate, and P. Nosil. 2015. Selection on a genetic polymorphism counteracts ecological speciation in a stick insect. Curr. Biol. (in press).

Gratten, J., A. J. Wilson, A. F. McRae, D. Beraldi, P. M. Visscher, J. M. Pemberton, and J. Slate. 2008. A localized negative genetic correlation constrains microevolution of coat color in wild sheep. Science 319:318–320.

Johnston, S. E., J. Gratten, C. Berenos, J. G. Pilkington, T. H. Clutton-Brock, J. M. Pemberton, and J. Slate. 2013. Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature 502:93–96.

Nosil, P. 2009. Adaptive population divergence in cryptic color-pattern following a reduction in gene flow. Evolution 63:1902–1912.

Nosil, P., and B. J. Crespi. 2006. Experimental evidence that predation promotes divergence in adaptive radiation. Proc. Natl. Acad. Sci. U. S. A. 103:9090–9095.

Sandoval, C. P. 1994a. Differential visual predation on morphs of Timema cristinae (Phasmatodeae:Timemidae) and its consequences for host range. Biol. J. Linn. Soc. 52:341–356.

Sandoval, C. P. 1994b. The effects of the relative geographic scales of gene flow and selection on morph frequencies in the walking-stick Timema cristinae. Evolution 48:1866–1879.

Sunday, June 28, 2015

Speciation, genomes, and pancakes

A decade ago, I began my PhD at Vanderbilt University in Nashville, Tennessee, where I was interested in studying the evolutionary process of speciation (or how new biological species evolve). I was very lucky during my PhD to be surrounded by great people. Case in point, I shared an office for part of the year with a visiting collaborator, Patrik Nosil, who studied speciation in a group of stick insects called Timema. Second, my PhD advisor encouraged me to invite great thinkers on speciation to be part of my dissertation committee – enter Jeff Feder from the University of Notre Dame, who studied speciation in a group of fruit-feeding flies called Rhagoletis and served as my external committee member. These connections made during the beginning of my PhD last to this day.

Figure 1. The Pancake Pantry in Nashville, TN, USA.
During a fateful visit to a common grad student hangout (circa 2007), the Pancake Pantry (Fig. 1), Patrik Nosil and I and a group of graduate students started discussing the age-old debate about the number of genes involved in adaptation (and speciation): few versus many? And whether the traits responsible for adaptation and speciation were polygenic traits or traits with a simple genetic basis? One way we thought to test this was to use as many molecular markers as you could survey, distributed across the genome, and ask the question: how many of these gene regions exhibit significant population differentiation, but are restricted to populations adapting to different environments? We came up with ideas of how to test it, and what type of tools we would need, right over our plates of pancakes! I think we even had a budget by the time we walked back in our calorie coma from lunch.  My major takeaway from this lunch was that I now considered the genome as an active player, not a passive mediator, in the speciation process and I would never think about speciation in the same way again!

What emerged initially from this pursuit were two comparative AFLP genome scans of two different study systems, each undergoing speciation driven by divergent ecology, that were published in the journal Evolution (Nosil et al. 2008; Egan et al. 2008).  These studies were very informative in highlighting the proportion of gene regions (AFLPs) in the genome exhibiting strong differentiation between divergent populations, and possibly addressed the repeatability of gene regions associated with adaptation to two environments (in our case, host plants).  But we were also left with many more questions than answers. How were these divergent loci distributed and arrayed across the genome? And were the loci exhibiting strong differentiation driven by selection or other evolutionary phenomena?

Fast-forward to 2010 – I finished my PhD and I was awarded a Faculty Fellowship at the University of Notre Dame, which came with some seed money for research and the chance to work more closely with my external committee member, Jeff Feder. Almost immediately upon arriving in South Bend, IN, Patrik (now in Sheffield, UK), Jeff, and I had a set of conference calls and email exchanges that started the project that would result in the Ecology Letters MS I will summarize below. (Jeff and Patrik had just finished a sabbatical in Berlin the year before where they spent much of their time ruminating on the genome-level phenomena influencing the speciation process.) We recruited other evolutionary biologists well trained in Rhagoletis biology (Tom Powell, Glen Hood, and Greg Ragland), as well as two computer scientists (Scott Emrich and his PhD student Lauren Assour) with the ability to process the large amount of data we would gather.

Our interests were to better understand the role the genome might play in the evolution of new species. We were inspired by a paper published over 30 years ago by Joe Felsenstein (1981), where he described the difficulty of building up many-locus differences between populations if gene flow was ongoing and recombination was breaking up associations. This conflict between selection and gene flow would form the basis for our project. How is it that populations can diverge in the face of ongoing gene flow? What are the properties or characteristics of species that are suspected of speciation-with-gene-flow which facilitated their divergence?

Figure 2. Rhagoletis pomonella exploring the fruit of the hawthorn tree (Crataegus mollis). Photo credit: Hannes Schuler
Rhagoletis pomonella offered a great study system to test these ideas, as it is a well-documented case of speciation-with-gene-flow (Fig. 2). Rhagoletis pomonella is a member of a sibling species complex containing numerous geographically overlapping taxa proposed to have radiated in sympatry by adapting to many new host plants from several different plant families. Rhagoletis flies infest the fruits of their host plants, where host fruits are typically available for a discrete window of time over the growing season and each fly species completes one generation per year. Adult flies meet exclusively on or near the host fruits to mate; females oviposit into the host fruit; larvae consume the fruit, then burrow into the soil to pupate, entering a pupal diapause that lasts until the following year. Thus, phenological matching of fly to host-plant fruiting is critical to fly fitness.

The most recent example of a host shift driving speciation is the shift of R. pomonella from its native host hawthorn to introduced, domesticated apple, which occurred in the mid-1800’s in the eastern United States. Genetic and field studies have shown that apple and hawthorn flies represent partially reproductively isolated host races and that gene flow has been continuous between the fly races since their origin. One key trait that differs between the races is the timing of diapause termination, which varies between the races to match the 3–4 week earlier fruiting time of apple versus hawthorn trees (Fig. 3). Rhagoletis emerge from their fruits as late-instar larvae and overwinter in the soil in a facultative pupal diapause. The earlier fruiting time of apples therefore results in apple flies having to withstand warmer temperatures for longer periods prior to winter. As a result, natural selection favors increased diapause intensity, or greater recalcitrance to cues that trigger premature diapause termination in apple flies.
Figure 3. Fruit on apple trees ripens 3-4 weeks earlier than hawthorn fruit (dashed lines). Apple flies eclose earlier as adults (solid lines) and are exposed to warmer temperatures as pupae in the soil for a longer period of time before winter.
Jeff had the perfect experiment frozen in his freezer from 20 years ago. Previously, his lab had reared the ancestral haw race of Rhagoletis under the phenological conditions of both host plants it attacks in nature. He had previously looked at changes in a set of allozymes and microsatellites, but did not have the ability at the time to look across the genome at tens of thousands of SNPs.  Specifically, he exposed ancestral hawthorn fly pupae to warm temperatures for a short 7-day (‘hawthorn-like’ control) vs. long 32-day (‘apple-like’ experimental) period prior to winter (Fig. 4).

Figure 4. In the selection experiment, hawthorn flies were exposed to a short (7-day) versus long (32-day) prewinter period to emulate the time difference experienced by hawthorn versus apple-fly pupae in nature. 
We also had a specific hypothesis we wanted to test that integrated Jeff’s selection experiment with sampling from natural populations. We tested whether the changes across the genome induced by the lab experiment on divergent host-plant phenology would predict the genome-wide differences observed at these same loci between natural sympatric populations. In this experiment, we stressed that we were quantifying the total genome-wide impact of selection, which involves both direct effects, where natural selection favors the causal variants underlying selected traits, and indirect effects, where additional loci respond because they are correlated due to linkage disequilibrium with these causal variants. Thus, the ‘total’ impact of divergent selection (i.e. direct + indirect effects) that we quantify here can involve changes at many loci (Gompert et al. 2014; Soria-Carrasco et al. 2014).

Quantifying the impact of selection genome-wide is important because, as populations diverge, the effects that individual genes have on reproductive isolation (RI) can become coupled, strengthening barriers to gene flow and promoting speciation (Barton 1983, Bierne et al. 2011). If predicated solely on new mutations, this transition could take a long time and populations could go extinct or conditions change without speciation, which may explain why sympatric speciation is difficult to observe and test. Thus, a prediction for systems with the potential for speciation-with-gene-flow is that they exhibit large stores of standing variation and consequently, show extensive, genome-wide responses to selection when challenged by divergent ecology.

In our selection experiment, about 6% of the SNPs showed significant frequency shifts between the short and long prewinter periods. However, because of extensive linkage disequilibrium (LD) in Rhagoletis, these SNPs did not provide an estimate of the independent number of gene regions influenced by selection. Thus, we assessed the pattern of LD between SNPs to delimit independent sets of loci.  We determined that the 6% of responding SNPs represented 162 different sets whose members were in LD with each other, but in equilibrium with all other SNPs. After accounting for the table-wide null expectation of 52 significant sets due to type I error, using a modeling approach we detail in our Supplemental material, a lower bound estimate of 110 gene regions responded to selection. To determine how physically widespread the response was across the genome, we constructed a recombination linkage map for Rhagoletis that contained 2,352 SNPs. About 13% of mapped SNPs showed significant frequency shifts in the selection experiment and were dispersed widely across the five major chromosomes of the R. pomonella genome (Fig. 5). Thus, numerous independent gene regions responded to selection and they were distributed throughout the genome.

Figure 5. Genome-wide comparison of allele frequency shifts in the selection experiment (red line; left axis) versus divergence between field-collected sympatric host races (blue line; right axis) along chromosomes 1-5. Circles above panels denote SNPs showing statistically significant response in the selection experiment (open red) or difference between the host races (solid blue). Correlation coefficient (r) is reported independently for each chromosome.
Now we tested our main hypothesis: does the genomic response in the selection experiment reflect nature?  The answer is yes. The direction and magnitude of allele frequency changes for all 32,455 SNPs in the selection experiment was highly predictive of genetic differences between the sympatric hawthorn and apple host races at the Grant, MI, site (r = 0.39, P < 10-6). Most strikingly, for the SNPs showing significant responses in both our selection experiment and host divergence in nature, the allele that increased in frequency in the hawthorn race after selection was the exact same allele in higher frequency in the apple race in nature (P = (½)154 = 4.4x10-47).

To what extent did the single bout of selection on hawthorn flies genetically create the derived apple race?  The answer is a good deal. For all 32,455 SNPs, the mean SNP frequency for hawthorn flies surviving the long prewinter treatment shifted 38.9% of the difference between the host races toward apple flies. For the 154 SNPs showing significant responses in the selection experiment and host divergence, the shift was 84.1%.

Why is the impact of divergent ecological adaptation so pronounced and pervasive in Rhagoletis?  One contributing factor is the extensive LD in the fly, some of which is due to inversions, requiring additional DNA sequence analysis to resolve. A second factor is the presence of substantial standing genetic variation in R. pomonella, which supports the hypothesis that such stores may define taxa having a greater capacity for speciation-with-gene-flow. Finally, when ecological adaptation involves traits like diapause that can be highly polygenic, selection may more often have genome-wide consequences. In this regard, microarray studies of R. pomonella have revealed hundreds of loci varying in expression during diapause breakage that are potential targets of selection (Ragland et al. 2011).
 
Figure 6. Rhagoletis pomonella fly exploring apple fruit. Photo credit: Andrew Forbes
Interestingly, this work shares some important similarities and differences with other recent studies combining selection experiments with surveys of genome-wide genetic variation in natural populations, including the Timema ecotypes that are the mainstay of the Nosil lab. In both a within-generation (Gompert et al. 2014; similar to the Rhagoletis study here) and a between-generation study of selection in the field (Soria-Carrasco et al. 2014), a genome-wide response involving many loci was observed. However, LD was much lower in the Timema ecotypes, and thus the association between genetic differences induced in those selection experiments did not match natural genetic variation as closely as in the Rhagoletis experiment.

In summary, divergent ecological selection can have genome-wide effects even at early stages of speciation. Large stores of standing variation in Rhagoletis flies may potentiate the evolution of genome-wide reproductive isolation and their adaptive radiation with gene flow. As the study of speciation genomics expands, it will be possible to test the degree to which other taxa prone to ecological sympatric speciation share similar characteristics as R. pomonella, and to assess the relationship between standing variation and clade richness.

That was one productive plate of pancakes!

References:

Barton, N.H. 1983. Multilocus clines. Evolution 37, 454471.

Bierne, N., Welch, J., Loire, E., Bonhomme, F. & David, P. 2011. The coupling hypothesis: why genome scans may fail to map local adaptation genes. Molecular Ecology 20, 2044–2072.

Egan, S.P., P. Nosil, & D.J. Funk. 2008. Selection and genomic differentiation during ecological speciation: isolating the contributions of host-association via a comparative genome scan of Neochlamisus bebbianae leaf beetles. Evolution 62: 1162-1181.

Egan, S.P., G.R. Ragland, L. Assour, T.H.Q. Powell, G.R. Hood, S. Emrich, P. Nosil & J.L. Feder. 2015. Experimental evidence of genome-wide impact of ecological selection during early stages of speciation-with-gene-flow. Ecology Letters, online early. (doi: 10.1111/ele.12460)

Felsenstein J. 1981. Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35:124 – 138.

Gompert, Z., A.A. Comeault, T.E. Farkas, J.L. Feder, T.L. Parchman, C.A. Buerkle, and P. Nosil. 2014. Experimental evidence for ecological selection on genome variation in the wild. Ecology Letters 17: 369-379

Nosil, P., S.P. Egan, & D.J. Funk. 2008. Divergent selection plays multiple roles in generating heterogeneous genomic differentiation between walking-stick ecotypes. Evolution 62: 316-336.

Ragland, G.J., S.P. Egan, J.L. Feder, S.H. Berlocher, & D.A. Hahn. 2011. Developmental 
trajectories of gene expression reveal regulatory candidates for diapause termination, a key life history transition in the apple maggot fly, Rhagoletis pomonella. Journal of Experimental Biology 214: 3948-3960.


Soria-Carrasco, V., Z. Gompert, A.A. Comeault, T.E. Farkas, T.L. Parchman, J.S. Johnson, C.A. Buerkle, J.L. Feder, J. Bast, T. Schwander, S.P. Egan, B.J. Crespi, & P. Nosil.  2014. Stick insect genomes reveal natural selection's role in parallel speciation. Science 344: 738-742. 

Monday, June 15, 2015

Old Monkeys in New Habitats: The Biogeography of Terrestrial Biotas.

I just returned last night (37 hours in transit!) from my first trip to Uganda. It was my second trip to Africa, with the first being to South Africa six years ago. The main purpose of the trip was to plan, with my colleague Lauren Chapman, some new studies on adaptation by fishes to extreme (low oxygen) environments. However, my first trip to any new location also becomes an adventure in natural history and photography. During these adventures, I was motivated to write a post based on a series of natural history anecdotes, which I will also seek to tie into a book I happened to reading at the same time.

Following in Lauren's foot steps.
My current bed time (and plane time) reading is The Monkey’s Voyage by Alan de Queiroz. The subtitle of the book is How Improbable Journeys Shaped the History of Life. The goal of the book is to contrast old and new views of biogeography, the study of where species are found and why. The old view is that the distribution of organisms and faunas across the world is almost entirely shaped by vicariance events that sunder formerly contiguous landmasses. These events including land masses splitting through continental drift, mountain ranges rising, large rivers forming, and so on. Under this view, the species found in New Zealand, for example, are remnants of an early Gondwanaland biota that persisted (and diversified) following the isolation of New Zealand from a larger land mass that included Australia. By contrast, the new view is that the distribution of terrestrial organisms is shaped to a larger extent by rare long distance dispersal across even large ocean distances. Under this alternative view, New Zealand’s fauna is mainly shaped by over-water dispersal from Australia long after the two islands split apart. (Interestingly, the new view is actually an even older view. Darwin spent considerable time studying mechanisms of long distance dispersal, although perhaps he wouldn’t have if continental drift had been known.) De Queiroz clearly favors the new view, marshalling extensive evidence that biogeography is strongly shaped by long distance dispersal.


Reading biogeography in books is interesting but experiencing it in person is transformative. For the last 14 years, most of my field work has taken place in South America, including Trinidad, Galapagos, Panama, and Chile, alongside shorter trips to Brazil, Barbados, Roatan, and other locations. Now my recent trip to Uganda, combined with my earlier South African trip, has brought home in a personal sense the differences between “New World” and “Old World” biotas.

A South African lion showing off his dental array.

A South African hippo showing off his even more impressive dental array.
The most in-your-face contrast, of course, would be the classic African large-mammal spectacles: elephants, hippos, buffalo, giraffes, lions, leopards, wildebeest, zebras, cheetahs, camels, and so on – most of which I have now seen in the wild. Although the New World certainly does have large mammals (moose, bison, bears, capybaras, tapirs, jaguars), they are not nearly as striking, abundant, or dramatic a spectacle. However, this contrast is somewhat disingenuous given that the New World had many similar forms (mastodons, mammoths, lions, sabre-toothed cats, camels) until their extinction in the Pleistocene not that long ago. (And, of course, bison recently did, and caribou still do, present huge migratory spectacles.) So, but for vagaries of our particular point in time, the large-mammal faunas of the two continents might not have seemed quite so different.

A brown bear from my cabin in Northern BC, Canada.

Yes, moose are huge - this one in Lake Nerka, Wood River Lakes, Alaska.
A classic contemporary contrast is Old World monkeys (and apes) versus New World monkeys. The two groups differ in a number of ways, including various aspects of facial shape and – iconically – the prehensile tail of New World but not Old World monkeys. In Panama, I have been able to observe howler monkeys, white-faced monkeys, spider monkeys, Geoffroy’s tamarins, and others. In Kibale National Park in Uganda, I was able to observe olive baboons, grey-cheeked mangabeys, blue monkeys, redtail monkeys, red colobus, black-and-white colobus, L’Hoest’s monkey, galagos (bush babies), pottos, and – the most amazing of all – chimps. (Kibale is said to harbor the highest primate biomass in the world.) Later at Lake Nabugabo, I saw vervets (more about these later), which I had also – along with baboons – seen in South Africa. Excepting chimps and baboons, and despite some differences in appearance, the two sets of monkeys strike one as superficially similar. They all move with varying degrees of frenetic activity through forest canopy feeding on a diversity of insects, leaves, and fruits. Thus, we here have a similar ecological set of organisms in the two worlds, with the new world monkeys having radiated from a single common ancestor colonizing the new world, perhaps by long-distance dispersal of just a few individuals from Africa (as argued by de Queiroz and others). 

Black-and-white colobus in Kibale National Park, Uganda.

Red colobus in Kibale National Park, Uganda.

Redtail monkey in Kibale National Park, Uganda.
Grey-cheeked mangabey expressing displeasure in Kibale National Park, Uganda.

Chimp mom with sleepy baby in Kibale National Park, Uganda.
For birds, the classic contrast is between hummingbirds and sunbirds. Hummingbirds, such a ubiquitous, striking, and engaging component of New World environments, are entirely absent from the Old World. Instead, the Old World has a large radiation of the nectar-feeding sunbirds. The first sunbird I ever saw was in Cape Town, South Africa. I was on Table Mountain composing a photograph of a flowering bush in the foreground with Cape Town in the background far below. In the midst of a sequence of photographs, a sunbird landed right in the middle of the flowers – almost as if I had planned for it. In Kibale and Queen Elizabeth Parks in Uganda, I saw more sunbirds. However, despite the similar ecologies and exuberant colouration of both groups, which are not closely related, no one would mistake one for the other. For instance, the hovering flight of hummingbirds – perhaps their most obvious feature – is relatively rare in sunbirds.

Bronze sunbird, Kibale National Park, Uganda.
Both continents have wonderful radiations of small colorful frogs. While traveling along the swampy edge of Lake Nabugabo, we had stopped so I could take pictures of birds when one of the field assistants pointed to a tiny yellow-and-black-patterned frog on a reed we were holding on to. Mediocre bird photos immediately forgotten, I switched to macro equipment and started taking endless photographs of the frog. Then, in the space of just a few minutes, he pointed out two other species of frog clinging to other reeds less than a meter away. All were colorful but in various shades and patterns of green. Moreover, they all froze in place and didn’t move no matter how close my hands got or how much I manipulated the reeds or stuck a macro lens in their faces. This appearance and behavior was a surprise after the poison-dart frogs that I had seen in Panama and elsewhere in the Americas. When I asked the field assistants if these frogs were poisonous, they did not think so. It seems this group has specialized on camouflage whereas the New World Dendrobatids have specialized on conspicuousness. (I am no frog expert – perhaps a radiation of poisonous and conspicuous frogs exists in Africa – and I am generalizing – some New World frogs are very cryptic.)

Lake Nabugabo frog #1, which I still haven't taken the time to identify to species.

Lake Nabugabo frog #2, which I still haven't taken the time to identify to species.

Lake Nabugabo frog #3, which I still haven't taken the time to identify to species.
We later visited another part of the swamp and the same field assistant found another small-and-green-themed frog of seemingly yet another species. At this point, I was starting to feel incompetent in my ability to find critters and decided that I would find my own damn frog. So I went walking slowly through the marsh scanning blades of grass and other vegetation. Half an hour later, having still had no luck, I was about to give up when I saw a bit of movement near the water. “YES” I yelled, “I finally found one of the buggers” and, then, looking closer, I saw it was actually a finger-length chameleon. Even better – my first ever chameleon; and I found it myself (considerable boasting followed). The next hour was spent taking 217 photographs of the chameleon plus additional shots of what appeared to be a fifth small-green frog species that another field assistant found. Chameleons are another major radiation in the Old World – especially Madagascar – that is completely absent from the New World, which instead has a radiation of Anolis lizards that are absent from the Old World.

My chameleon. Found at Lake Nabugabo, Uganda.

Getting a closer look at my chameleon. Found at Lake Nabugabo, Uganda.

Lake Nabugabo frog #4, which I still haven't taken the time to identify to species.

Lake Nabugabo frog #5, which I still haven't taken the time to identify to species.

To these Old versus New faunal contrasts that I already knew, the present trip added another. After having seen and photographed most of the diurnal primates, Lauren took me on a night walk to look for the nocturnal primates. Almost immediately, we saw a potto, which I am told is not common, and I was able to get some photographs with a long lens and flash. What immediately struck me about the potto was its slow, branch-hugging movement; kind of like a sloth. Hmmmm, what about sloths? Sure enough, Lauren confirmed that sloths are absent from the Old World just as potto-equivalent primates are essentially absent from the New World (although the latter does have night monkeys). 

Potto doing its sloth imitation in Kibale National Park, Uganda.
In this post, I have been a Natural History Tourist, giving my own superficial impressions of some differences between the two “worlds.” Although these impressions are based on relatively little experience in Africa, they made me ponder the biogeography debate I had been reading in de Queiroz’s The Monkey’s Voyage. Long distance over-water dispersal has certainly shaped the world’s fauna but vicariance ultimately seems more important through its role in limiting movement between land masses. On the one hand, long-distance dispersal does happen and is critical in shaping species distributions: without it we would not have any organisms on oceanic islands and many iconic organisms of large islands and continents would also be missing, including perhaps monkeys in the New World. On the other hand, faunas differ so much from place to place that effective long-distance dispersal must be very rare and vicariance provides the dominant factor assembling many communities.

I doubt de Queiroz would disagree with these points even though his book is very much focused on long-distance dispersal. Another way to explain the distinction is that long-distance dispersal is critical for explaining why species ARE in particular places whereas vicariance is critical for explaining why species ARE NOT in particular places.

All of this brings me back, believe it or not, to vervets, the first monkey I ever saw in the wild. This statement might seem surprising if you remember that vervets are Old World Monkeys whereas I had worked in South America for eight years before visiting Africa. In fact, my first experience with wild monkeys – the vervets – was in 2003 in Barbados. Yes: Old World Monkeys on New World Islands! It turns out that vervets were brought about 350 years ago to Barabados and some other Carribean islands by slavers. I don’t think other monkeys are naturally found on those islands, at least not on Barabados, so this isn’t a lesson in what happens when the two faunas collide. But if they did collide, who would win? Are New World Monkeys “better” than Old World monkeys? (They have that cool tail!) Would New World monkeys win in the New World and Old World monkeys win in the Old World (local adaptation!) – or vice versa (enemy release!)? Of course, countless such experiments are being undertaken with other organisms, as the field of invasion biology attests, but I don’t know any examples of recent human-mediated conflicts between ecologically-equivalent iconically-divergent faunas such as those described above. (Although placental dingos replaced, whether causally or not, the marsupial thylacine in Australia).


A Barbados vervet
How interesting it would be to bring hummingbirds to the Old World and sunbirds to the New, Anolis lizards to the Old and chameleons to the New, capybaras to the Old and hippos to the New, and so on. (Apparently Pablo Escobar, the drug lord, had a hippo herd that is now feral and expanding in Columbia.) Just think how much we would learn and how fun it would be to see the dynamics play out. Sadly, however, the likely ecological impact would exceed the value of the information gained thereby. I would much rather see Anolis in South American and chameleons in Africa than I would like to find out who would win in direct competition in nature. It is too bad we can’t have replicate worlds, some for conservation and some for experimentation.

Grey-crowned crane at Lake Nabugabo, Uganda.