Monday, 29 July 2013

Impossible realities: adaptive radiations and the suspension of disbelief

[This post also appears on my other blog:]

Adaptive radiations occur when a single ancestral species radiates into multiple descendent species as a result of adaptation to different environments or resources. Adaptive radiations provide perhaps the clearest evidence for the role of adaptation in shaping the diversity of life – think Darwin’s finches in Galapagos, Anolis lizards in the Carribean, figs and fig wasps, Hawaiian silverswords, and so on. The typical assumption of this model of evolution is that a number of empty “niches” exist and that organisms evolve and speciate to fill them, after which the radiation ceases. However, a number of alternative possibilities exist, such as the evolution of one species creating a brand new niche that favors the evolution of still more species – diversity begets diversity.

These possibilities have been explored using a variety of methods. One method is to try to figure out how many possible niches are out there – and how many of them are filled. That is, do the 13 or so species of Darwin’s finch correspond to the 13 different resources to which finches can possible adapt? Stated another way, is the fact that marine finches and cave finches don’t exist mean that these niches are not accessible to finches or that finches simply haven’t gotten there yet? 

Questions along these lines are often explored by investigators attempting to guesstimate what niches are possible for a given taxonomic group, thus enabling estimates of which niches have and have not been filled by a given adaptive radiation.  But how does one establish the range of possibilities? That is, how does one determine whether a hypothetical niche (marine finches) is or is not possible (i.e., accessible to the adaptive radiation)? A common route to this determination is to estimate the range of biomechanically possible morphologies and then determine how much of this range is filled by extant organisms. Unfilled morphospace then means the radiation hasn’t yet been completed – empty niches are still in waiting.

Sometimes I fear that these endeavors are doomed to failure – because it is usually impossible for us to determine what realistic empty niches are out there but have not yet been filled. This opinion first crystallized for me on my first trip to Africa and was brought back to mind by this week’s trip to sample guppies in Trinidad. The key realization for me was that many organisms that currently exist would probably not have been considered possible if they hadn’t already existed. The most obvious examples of these impossible realities are situations where one or a few species are highly divergent in morphology from other organisms – with giraffes first bringing the point home to me. Giraffes are so different from other organisms that I would bet that we would never imagine they could exist if they didn’t already. Ditto for hippos and bombadier beetles and aye-ayes and emperor penguins and mudskippers and cookie-cutter sharks and gastric brooding frogs and hydrothermal vent organisms and so on. In other cases, it is a whole group that is so bizarre that we wouldn’t believe them without the proof staring us in the face. Perhaps most striking, no one imagined dinosaurs – at least not in the depth and breadth of their majesty – before they had been revealed by fossils.  And I would place deep sea angler fishes in a similar place. These bizarre creatures suggest to me that many other morphologies, presumably suited for very divergent niches, still exist out there and have not been filled.

Beth and Felipe catching guppies.

The reason my trip to Trinidad brought this point back to mind was that a species exists there that is so bizarre as to challenge credulity, except of course for the fact that it actually exists. Imagine a bird that lives in caves (some other birds – cave swiftlets – also do so), feeds at night (some other birds – nightjars – also do so), has chicks that can be melted down to make oil, and echolocates (….). Yes, indeed, they echolocate. They use a series of clicks and screeches to help them navigate in pitch darkness both inside and outside of their caves. Bats do it, but birds? Bizarre. Unprecedented. Impossible? I had long heard about oilbirds and had even seen (mostly heard) them fly by while camping at night in remote rivers of the northern range of Trinidad – but never before in 13 years of visiting Trinidad had I seen them in their caves. But this was finally that year, with Felipe Perez leading me on a 2.5 hour hike up into the mountains to one of their (few) caves.

From my field notes: We reached the cave well after dark and were coaxed along the last few hundred meters by an ever growing crescendo of loud clicks and screeches. We wormed our way down a tiny creek in a small canyon and into a boulder field that descended into the mouth of the cave. The cave was quite large and extremely noisy and a bit smelly and wet, with water dripping from the cave roof. It was not a horizontal cave like you see in the movies but rather seemed to go about 45 degrees down and into the depths – presumably having been wrought by the creek flow over eons. Along the walls of the cave were ledges that were full of screaming oilbirds. [Wikipedia notes: In Trinidad it was sometimes called diablotin (French for "little devil"), presumably referring to its loud cries, which have been likened to those of tortured men.] They would either sit there and hurl imprecations or fly back and forth in and out of the cave opening or around inside the cave. It was quite spectacular and I wasted no time in getting out the camera. The photography conditions were quite difficult, however, as it was pitch black and the oilbirds were mostly far away – so Felipe would hold both headlamps pointing at a bird and I would use a telephoto with a big flash, which – after much trial and error – took some decent photos.

Echolocating oilbird.

Although oilbirds were the main reason I was reminded of the difficulty of identifying the possible in evolution – and although they fit the illustrative point of a specific bizarre species very different from all their relatives – I can’t help but also mention a very different scenario that tells the same story on a much grander scale. That is, an entire group that seems familiar to us only because of their existence – snakes. By this I mean that – if snakes didn’t exist – we might be hard pressed to imagine their existence, although some legless lizards get pretty close. But, in reality, I am particular motivated to mention snakes – and to think about their strangeness – because of a recent encounter in Trinidad.
Fer-de-lance: the snake we most commonly encounter in Trinidad.

From my field notes: I was processing fish at the table in Simla (the William Beebe Tropical Research Station) and had just finished a tank of fish. I picked up the tank to take it and empty it outside and was walking out the door when “thump” something heavy fell in the area between the open door and the door jamb. I looked quickly and saw it was a very big snake. Thankfully, I also instantly saw that it wasn’t a poisonous one – or at least not a poisonous one I was familiar with – so I just kind of backed off and called Felipe and Beth to come have a look. During this time, the snake, which turned out to be Pseustus sulphureus sulphureus, was slowly working its way up the door jam and higher toward the rafters of Simla. Felipe quite correctly pointed out that it would be good to not let it get too high above our reach or we would never get it – so I ran and got some butterfly nets to catch it. Felipe then engaged in a protracted dance with the snake to try to catch him in the nets, which he eventually did. I kibitzed and took photos and videos. After taking it outside, we let it go and it sort of hung around in some bushes nearby. We were confident its traumatic capture, handling, and release would convince it to depart.
Knock knock
Getting higher
Pest removal by Felipe.
Now that's a big snake (Pseustus sulphureus sulphureus)
About 15 minutes later, I was sitting having lunch on a couch facing the open door when, what should I see but the snake slowly slithering back inside the door. This time it was my turn to take a stick and pick the snake up and deposit it farther away from the house. But, by this time, I was starting to think that maybe it really wanted to be in the house and that it would not be deterred. Sure enough, about 15 minutes later, Felipe found it right beside the house again. This time, we moved it into the trees a bit away from the house, just the sort of habitat where it should like to be. It stayed there initially but I was getting more confident that it would be back – so I kept an eye on it. In fact, I went and got my camera to take some more photos – this time in its more natural environment. By the time I got back outside, I could see that it was starting to move out of the trees again toward the house. So I started filming.

As it got closer and closer, it changed direction and was heading right for me. Hmmm, this will be a good video, I thought. Then it came out of the tree not two feet in front of me – heading straight for me. A good video indeed! In fact, I could see that it was still heading toward the house, which was behind me, and the most direct route from where it was to the house was directly between my legs. I kept filming and, sure enough, it kept going right through my legs and toward the house. I eventually stopped filming because I could see it was about to enter the house through a small hole, so I grabbed its tail and it instantly whipped around and struck at me. Being at about waist height on some steps at that point, it definitely raised my adrenalin level. 
You lookin' at me punk?

By this point, I was really enjoying the snake but also finding it quite distracting – I had fish to process after all. So at the end of this third encounter, I collected it with a pole and dropped it off a rather steep – if short – cliff lined with ivy. Although it clearly wouldn’t be injured, I figured it would at least get the idea that it might get injured if it stayed. It wasn’t that I was afraid of the snake or didn’t like it – quite the contrary – I just figured that it would be very distracting if we were having to keep our eyes open all the time while we were in the house for fear of stepping or sitting on it. Remember sitting on your house cat by accident, well this would take it to the next level.
Pseustus sulphureus sulphureus

After this most recent encounter, I went back to work processing guppies, but I kept looking behind me toward the door and windows because I was still thinking it might be back. Sure enough, about 15 minutes later, I could see it climbing the outside of the house and then entering the house along the edge of the vaulted rafters about 3.5 m up. Then it proceeded to move along this edge. Well, I thought, we can’t have it moving up into the attic or down into our rooms – that would take the distraction to a whole new level, so I set out to corral it in the same way Felipe had done previously. But now it was about a meter higher than before, so I had to stand on a desk or table and reach way above my head with the nets trying to get the snake into the net. This I could sort of do – but only the first half of the snake – try as I might I couldn’t pry the other half off the edge – and it became rather exciting when it would turn around and coil up as if to strike – while being 1 m above my head looking down at me.
As I didn’t succeed in capturing it, it turned around and went the other direction until it got to a new place where I could take another whack at it. Back and forth and back and forth we went in some bizarre pas de deux. Each time I tried to catch it, it would turn around and head the other direction. I would then sit down to process a few fish and, then, when it finally reached somewhere new where I could get at it, I would rush over, jump on the table (or desk) and try to corral it again. It eventually seemed to tire of this game and worked its way out of the house and onto the roof. That was it for that day but I suspect that the next visitor to Simla will have a similar adventure.

Another Trinidad oddity - the endemic Mannophryne trinitatis and his tadpoles.

So, from snakes to oilbirds to dinosaurs to hippos to giraffes, it seems to me that the human imagination and even calculation is incapable of postulating the possible endpoints in an adaptive radiation. We either circumscribe the possible morphospace much more than the actual reality, or we postulate things that really aren’t possible no matter what.  I am not sure where this leaves the study of adaptive radiation except perhaps to the idea that the best judge of what is possible is what already exists, with the caveat that this is almost surely an underestimate of what is actually possible. Adaptive radiations are indeed stranger than fiction.
Here are some more pictures from the Trinidad trip:
Here is my Trinidad post from last year:

Tuesday, 2 July 2013

NEO Symposium Abstracts


Galaxias eclipsed by aliens

Abstract: In the realm of galaxiid fishes (Galaxiidae) in cold-temperate freshwaters of the Southern Hemisphere, understanding the ecological impacts of invasive salmonids (Salmonidae), especially brown trout and rainbow trout, is a priority to develop conservation guidelines and learn about the diversity and function of natural ecosystems. Galaxiids are considered amongst the most seriously threatened fishes known presumably due to trout invasions, but data is often qualitative and ambiguous. Furthermore, little is known about the extent to which native ecosystems have been transformed, especially in lakes. The goal of my PhD thesis was to fill some of these knowledge gaps by investigating Patagonian lakes. The results showed a strong effect of trout on the decline of Galaxias platei, as well as a natural constraint to trout invasions (impacts) that results in valuable yet insufficient ecological refugia. At the individual level, trout and G. platei affected each other’s trophic niche asymmetrically—trout escalated whereas G. platei sank in the trophic chain, a perspective rarely studied. Finally, the invasion created a natural experiment suitable to demonstrate a strong negative top-down control on zooplankton elicited solely by G. platei. By contrast, trout, by reducing the abundance of galaxiids, had a strong positive top-down control on zooplankton. This talk will be spiced up with footnote slides addressing additional issues related to methodologies, conservation, management, and environmental policy, in an attempt to showcase the diversity of perspectives and approaches that NEO students are prone to navigate.


On sex and the evolution of parasite resistance: does sexual dimorphism prevent parallel evolution?

Abstract: Populations that are spatially segregated often experience different selective environments, which cause the adaptive divergence of traits that influence survival and reproduction. When this occurs in a similar fashion for multiple independent population pairs, the outcome is called “parallel” evolution. Recently, increasing emphasis has been placed on the fact that populations in similar environments often differ substantially in adaptive traits, suggesting an element of “non-parallel” evolution. Similar questions surround adaptation by the two sexes to divergent environments. Parasites are an important selective agent known to cause adaptive divergence between populations; how host resistance (the ability to reduce or control parasite numbers) evolves is a key issue in multiple fields. We explore whether males and females in the same population respond differently to a similar shift in parasite pressure. On the one hand, parasites often have similar effects on males and females and the genes that influence resistance to specific parasites are often found on autosomes, suggesting that a shift in parasite pressure might lead to parallel (or symmetric) evolution of the sexes. On the other hand, males and females often experience different parasite levels, have different costs of infection and different costs of defence. We tested guppies (Poecilia reticulata) that were released from selection by a key parasite (Gyrodactylus spp.) in four replicate translocations in the wild. After four and eight generations, guppies from the translocated populations, and from the source population which remained exposed to Gyrodactylus, were sampled and bred to second generation under common garden. We exposed these descendants to individual infections with G. turnbulli and monitored parasite numbers on isolated guppies over a period of 24 days. The release of wild fish from Gyrodactylus led to asymmetric (non-parallel) evolution of resistance in the sexes: females derived from three of four translocated populations showed increased resistance relative to the source population, whereas males showed no change.


Supervisors: Mark Torchin (STRI) and Andrew Hendry (McGill)

Infection preference and host specificity of an invasive parasite to novel invasive hosts in the Panama Canal: natural experiments in ecology and evolution of adaptive specialization in a human-dominated invaded landscape.

Abstract: Host range, or the breadth of species that a parasite or pathogen can infect, is an important life-history trait that determines the ecological impact of a parasite and elucidates evolutionary trajectories of biotic interactions. Trematode parasites have complex life cycles with varying degrees of host-specificity, such that they are less specific to second intermediate hosts than they are to first intermediate snail hosts. Here, we investigate the extent to which exotic parasites interact with an assemblage of invasive species in order to understand the role of biological invasions in facilitating the transmission of these parasites through ecological and evolutionary processes. Specifically, we investigate how a globally widespread and economically important invasive parasite, Centrocestus formosanus, interacts with an assemblage of invasive snails with which it does and does not share a common evolutionary history. We also investigate how it interacts with a novel community of native cichlid fish in the Panama Canal that can serve as potential second intermediate hosts. We report that in natural assays of prevalence and in preference experiments in the laboratory, infection of Cichla ocellaris was significantly higher than other co-occurring cichlids. Single species experiments also demonstrate a higher infection rate for this fish than other available hosts. We speculate that the observed preference of C. formosanus on C. ocellaris, a popular sport-fish, demonstrates local adaptation to an invasive host in the Panama Canal. Infection preference for novel invasive hosts can thus have significant consequences for the transmission and evolution of emerging parasitic diseases. We hope to continue this research by evaluating patterns of host preference and parallel local adaptation to invasive and aqua-cultured fish species in other parts of the world in understand the processes that drive rapid local adaptation of infectious agents in invaded, human dominated landscapes.


Supervisor: Sylvie DE BLOIS1, and Gerardo CEBALLOS2
1  Plant Science and School of Environment, McGill University. Montreal, H9X 3V9 Canada
2 Ecology Institute, National Autonomous University of Mexico. Mexico city, 70-275 Mexico

Bridging the gap for large cats: connecting the dots for ecological corridors of a complex habitat for the jaguar in Mexico.

Abstract: Current trends in biodiversity conservation are based on maintaining suitable habitat conditions not just within protected areas, but also on adjacent, sustainably managed lands. This is especially challenging for the conservation of large carnivores such as the jaguar that require connected habitats to minimize extinction risks and facilitate movement while minimizing conflicts with humans. This study provides spatially explicit habitat information for jaguar management and the implementation of corridors linking its populations in the Yucatan peninsula, Mexico, an area of international significance for the species. First, habitat suitability models based on jaguar occurrence records and a combination of land use and land cover (LULC), distance to infrastructures (human settlements and roads), and climate (mean annual precipitation) were constructed using MaxEnt. Then, this information was used to derive a cost surface for mapping suitable corridors, linking four locations (nodes) where current jaguar observations were concentrated. Five potential corridors of varying quality have been identified between the population nodes in the biosphere reserves in the peninsula, the best one being from south to northeast along the Caribbean coast. The corridor connecting northern locations from west to east had the poorest habitat conditions. The suitable habitat models and corridors support the potential value for conservation of productive lands under sustainable forest management since most potential suitable habitats for jaguars were found outside protected areas. These results can be useful to highlight areas of potential opportunities or conflicts for jaguar conservation in a human-dominated landscape and to target areas for further jaguar surveys.


Remittance Cultivated Landscapes: Land use change, forest recovery, farming decline, and new trends in a Zapotec town of the Sierra Norte of Oaxaca, Mexico

Abstract: In indigenous towns, high levels of emigration have led to rapid shifts in economy and landscape. Such is the case of Yalálag, a Zapotec town in the Sierra Norte of Oaxaca, Mexico. Many Yalatecans have observed transformations in landscape composition over the past three decades due to a dramatic decline in farming activity. In this presentation, I show how land-use change is related to emigration but also to broader economic changes and state-policies. As a result, there have been intentional changes to social organization and norms around the use of natural resources that, on the one hand, has led to increased forest conservation but, on the other, has led to conflict with settlements on the periphery of the town’s borders. Moreover, I show how land-use change has caused a dependency on external food sources and affected the Yalatecan diet. Thus my presentation will aim to link the ecological, social, and cultural dimensions of transformations in Yalálag’s landscape.


Title: Leaf traits and specialist herbivores on Zamia elegantissima (Zamiaceae)

Abstract: Neotropical cycads protect their leaves against insect herbivores with different chemical and mechanical barriers. Specialist herbivores have means to cope with these defenses; however, the extent that leaf traits limit the activity of these well-adapted specialist insects is unknown. In this study, we have investigated the incidence of specialist herbivores and changes in leaf traits of the Panamanian cycad Zamia elegantissima. Herbivore incidence and leaf traits related to herbivory, such as leaf age, lamina thickness, resistance to fracture, work to fracture, chlorophyll content, water content, trichome density, and toxic azoxyglycoside (AZG) content were measured throughout leaf development. Principal Component Analysis of leaf traits identified characteristics that may explain specialist herbivore incidence. Z. elegantissima leaf development is characterized by quick leaf expansion and delayed greening. Young leaves are protected by trichomes and AZGs, but these defenses rapidly decrease as leaves expand. Decreases in AZGs are correlated to increases in lamina thickness and leaf toughness. Specialist herbivores feed on leaves for a discrete window of time (10 to 100 days after leaf flush) and consume 36% of total leaf production. AZG levels between 5–200 mM/g are correlated with herbivore incidence, however, at extreme levels (>500 mM/g) herbivory was absent. Herbivory by specialist is constrained during leaf development; young leaves are chemically protected and older leaves are physically protected. Our results support the hypothesis that chemical defenses still limit the activity of specialist insects. However, as leaves age, AZG levels decrease and toughness becomes a primary mechanism to deter herbivores.


Latitudinal Gradients in the Parasitism of the Invasive Lionfish (Pterois volitans) in the Caribbean

Abstract: The biotic resistance hypothesis (BRH) posits that resident species can limit the demographic success of introduced species through herbivory, predation, competition, and parasitism.  Biotic resistance to biological invasions is hypothesized to be strongest at low latitudes due to higher native diversity and stronger biotic interactions. We have examined this hypothesis by comparing the abundance, species richness, and effect of metazoan parasites infecting the invasive lionfish (Pterois volitans) across 13 sites in the western Atlantic, encompassing 17 degrees of latitude. The invasion by the lionfish presents a unique opportunity to test predictions regarding latitudinal patterns of biotic resistance to invasion due to its rapid spread and broad geographical distribution.  We predicted that the diversity and abundance of parasites infecting P. volitans would be highest at low latitudes, and that higher parasitism at low latitudes would have a negative effect on the condition of the host. Overall, P. volitans were infected by few parasites.  Though parasitism was relatively low in lionfish, species richness and abundance of ectoparasites was significantly higher at low latitudes; meanwhile no such pattern was observed for endoparasites.  Furthermore, we did not find an association between parasite abundance (within or across parasite groups) and host condition at any site.  These results suggest that although lionfish are more parasitized at low latitudes, they experience little resistance from native parasites across their introduced range.  Results from this work correspond with the findings of previous studies on latitudinal patterns of parasitism for native marine fish.  This suggests that factors other than host-parasite evolutionary history may also play a role in structuring observed latitudinal trends in parasitism.


The role of predators on the evolution of electric fish signals.

Abstract: Brachyhypopomus occidentalis is a weakly electric fish that produces electric signals for navigation, prey location and communication. Recent studies have shown that populations of B. occidentalis across Panama are diverging in the shape of their electric signals, but we do not know if these modifications have been driven by selection. Electroreceptive predation has been proposed as a major selective force shaping the electric signals of weakly electric fish. The main objective of my research is therefore to investigate if electroceptive predation has been driving signal divergence in B. occidentalis.


Supervisor: Catherine Potvin

The good dweller's dilemma: A land tenure and forest cover analysis in Panama and its
implications for REDD+ implementation

Abstract: Conserving forest carbon stocks in forested areas of developing countries is an essential component for REDD+ yet IPCC guidance focuses on emissions and removals from the Land Use and Land Use Change and Forestry Sector. Using recent land cover maps, we assessed and compared different land tenure regimes in Panama with respect to forest cover and forest cover changes through time. We found that protected areas and indigenous territories, which collectively represented 77% of Panama's total mature forest area in 2008, had the highest forest cover and lowest deforestation levels. While protected areas and indigenous territories in Panama have shown similar forest coverage from 1992-2008, the lowest deforestation rates were found where indigenous territories comarcas and claimed lands) and protected areas overlapped. Our results suggest that in the future national REDD+ strategy, government investment providing incentives for REDD+ should strengthen existing protected areas and increase participation of indigenous peoples in REDD+ efforts. We discuss the implications of this finding for the establishment of a reference level and examine possible financial incentives that could contribute to the Panamanian REDD+ strategy. The discussion is relevant to high forest cover/low reforestation rate countries and jurisdictions. Recognition of good stewardship in national and international contexts will indeed help to maximize the effectiveness of REDD+ by reducing potential leakages and promoting equity in the program.