I am interested in whether, how, and why ecology shapes evolution (and evolution shapes ecology) through time, with an emphasis on microevolutionary pattern and process, adaptation, and field experiments. I completed my Ph.D. on Anolis lizards in the Department of Organismic and Evolutionary Biology at Harvard University. I am currently a post-doctoral researcher at the University of Texas, Austin studying threespine stickleback. They're not anoles, but they're cool too.
It’s common wisdom that formalin-preserved samples can’t be DNA sequenced because formalin degrades DNA beyond use . However, a paper recently appeared in Genome Research, describing successful whole genome sequencing of formalin-prepared samples.
If it is possible to sequence DNA from formalin-fixed specimens, then that opens up a world of genetic studies through space and time using museum specimens.
However, the samples in the Genome Research paper, besides being formalin fixed, were also paraffin-embedded, and probably deep-frozen, as they were cancer research archival samples. Paraffin embedding and deep-freezing may also be required for successful sequencing of formalin fixed samples. Thus, perhaps the method won’t work for samples stored for 75 years at room temperature.
I don’t have the expertise to say. Any of our more molecularly savvy readers care to venture?
If there is any DNA left behind, say after a short formalin fix followed by ethanol storage, then DNA sequencing of formalin-preserved samples should be the equivalent of ancient DNA approaches, no?
CITATION: Scheinin, Ilari et al. 2014. DNA copy number analysis of fresh and formalin-fixed specimens by shallow whole-genome sequencing with identification and exclusion of problematic regions in the genome assembly. Genome Research 24: 2022-2032. doi: 10.1101/gr.175141.1
The first Anole Annals post, as Anthony Geneva reminded us a few days ago on AA’s fifth anniversary, consisted of a few anole-related haikus. One of them was:
Dewlap and Toepad.
Adaptive Radiation.
Key Innovations?
Key innovations are traits that are thought to enable lineages to diversify greatly, as these traits are adaptations that remove constraints and allow lineages access to new niches and adaptive zones. In anoles, the dewlap is considered a key innovation as it provides greater potential for diversity in signaling traits important for mate and species recognition, thereby increasing the rate of speciation across Anolis.*
The toepad is also thought to be a key innovation. Toepads allow anoles to climb on smooth surfaces. By climbing, anole species can partition the habitat not just in horizontal space, but vertical space as well. Thus, toepads have opened the arboreal niche to anoles, thereby playing a likely role in Anolis community assembly during adaptive radiation.
Several lines of evidence support the toepad’s role as an adaptation to arboreality. (1) Large toepads do tend to be found on those anole species that live higher in the canopy; (2) larger toepads impart better clinging ability; and (3) a recent study showed that populations of A. carolinensis that shifted to higher perches rapidly evolved larger toepads.
However, anoles also have claws.
As anyone who has ever had a cat jump onto their head knows, claws are also useful for climbing. Claws can interact with surfaces by interlocking with surface irregularities, or through friction, and the morphology of the claw determines in part how useful it is for climbing. Very few studies have been conducted on the Anolis claw, however, so we don’t have a good sense for whether and how anoles use the claw during climbing. We also don’t know how the claw might co-evolve with the toepad, if it does. Thus, the role of the claw in anole evolution, and its relation to arboreality, remains unknown.
To that end, Crandell et al. investigate the claw (and toepad) in a new paper just out in Zoology. They find that the toepad doesn’t tell the whole story of Anolis climbing. Perhaps, the claw also determines which Anolis have to stay on the ground and which can go into the trees. Read on…
Hey, that’s not an anole! American Rubyspot Damselfly (Hetaerina americana). Copyright Steve Collins
My colleagues and I recently published a paper documenting character displacement in Anolis carolinensis following the invasion of A. sagrei into Florida. The former moved up into the trees and evolved larger toepads. We did a lot of work in that paper to show with a high degree of certainty that the interaction between the two species is what led to character displacement in A. carolinensis. However, an open question remains as to exactly what kind of interaction, or interactions, they share. Most likely, the two species are competing for food (i.e. exploitative competition). They may also be interacting indirectly through a shared predator or parasite (i.e., apparent competition), and they are known to eat each other’s hatchlings (i.e., intraguild predation).
Today, I’d like to explore another possible interaction in depth: perhaps the two species have diverged to lessen aggressive interspecific interactions for space and territory (i.e., interference competition). For more, let’s turn to the anoles of the Odonata world (provocative statement, I know!): rubyspot damselflies (Hetaerina spp).
Previous work [1,2,3] in Grether’s group had shown that male competitor recognition in rubyspot damselflies depends on hindwing coloration, and that cross-species recognition and male wing coloration diverges between species living in the same area. This suggests that aggressive interactions between males of different species have driven divergence in wing color to reduce the frequency of energy-intensive, aggressive interactions between species. This divergence is consistent with a type of character displacement called Agonistic Character Displacement (ACD), which is the divergence between species in some sort of species recognition trait to lessen the negative effects of aggressive encounters.
However, another type of character displacement, Reproductive Character Displacement (RCD) is also consistent with these previous findings. RCD is divergence, usually in some sort of mate recognition trait, between two species. By diverging in such a trait (think anole dewlaps), males and females of different species are less likely to spend precious time courting or mating in wasteful, failed cross-species reproductive efforts.
By this point, you, the astute reader, may have noticed that both ACD and RCD predict changes in signaling traits–the former species recognition traits, and the latter mate recognition traits.
Whenever the same trait functions as a signal for both species and mate recognition, and that does happen often, telling apart the action of these two distinct processes (i.e., selection to reduce wasted aggressive effort versus selection to reduce wasted reproductive effort ) can be very difficult*.
Drury and Grether designed a very nice test for successfully discerning between these two hypotheses.
In a recent paper in The American Naturalist, Martha Muñoz, Johanna Wegener, and Adam Algar noted an interesting pattern in two clades of Caribbean anoles evolving independently on Cuba and Hispaniola: high elevation species tended to have smaller body sizes than lower elevation species*.
Figure 1: Body size-elevation relationships in Hispaniolan (cybotes clade) and Cuban (sagrei clade) anoles. The x-axis is elevation in meters (on the log scale). The y-axis is SVL, or snout-vent length, a measure of size. The colors represent individual species within each clade; grey represents A. cybotes and A. sagrei on Hispaniola and Cuba, respectively.
Having found that the two groups converged independently on a similar evolutionary pattern, the authors wanted to know: was the underlying evolutionary progression also the same?
To answer this question, the authors took advantage of the fact that the two clades harbored multiple species. By measuring body size-elevation patterns within each species, and then asking how those patterns combined with interspecific patterns to create the overall body size-elevation cline (SEC) observed across all species, Muñoz & Co. could discern subtle differences between clades in the evolutionary trajectory towards convergence. For example, one clade might build its overall size-elevation cline by having the same SEC relationship present in each species, with species also sorting themselves by elevation and size (Model H1). Whereas another clade might build its size-elevation cline just through interspecific differences in size and elevation, without an SEC relationship within species (Model H2).
Figure 2: Two models, of eight that the authors proposed, which might explain how body size-elevation clines evolve. Within-species clines are represented by different colored/dashed lines. Across-species clines are best visualized by drawing an imaginary line through average size and elevation of each species . In H1, each species has the same size-elevation relationship (i.e., the negative slope) and is found at different elevations. This creates a size-elevation relationship that depends on both intra- and interspecific patterns. In H2, each species has no size-elevation relationship (i.e., the flat slope) but is found at different elevations. Here, the size-elevation relationship is driven purely by interspecific differences in elevation and size.
The authors developed eight models for how elevation and size might be related within species and across species. They tested which of those eight models best explained variation in the relationship between size and elevation within species and clades, while accounting for spatial autocorrelation among collection localities and differences in elevational range among species . They then compared best models across clades to see whether convergence was reached by similar or different evolutionary pathways.
What did they find?
Figure 3: Intra-specific size-elevation clines (SECs) for Hispaniola (left panel) and Cuba (right panel). Solid lines represent significant SECs; dashed lines represent non-significant SECs.
On Hispaniola, each species tended not to show any significant intraspecific SEC relationships: note the flat slopes of the dashed lines in the left panel of Figure 3. Instead, much of the overall SEC comes from interspecific differences in size and elevation, consistent with Model H2 (Figure 2).
On Cuba, in contrast, the authors found some significant within-species SEC relationships–the solid lines in the right panel of Figure 3–but found that interspecific differences in size and elevation explained very little of the clade’s overall SEC (Figure 4)**.
The model most consistent with the Cuban data.
Thus the authors answered their question: “Although the precise mechanisms underlying inverse size[-elevation] clines remains unknown, it is clear that they were constructed in different ways on Cuba and Hispaniola.” In other words, the two clades show a pattern of convergence to small size, but they took different routes of intra- and interspecific evolution to get there. It reminds me of Yogi Berra’s response when asked directions to his house: “When you get to the fork in the road, take it!”
CITATION: M.M. Munoz, J.E. Wegener, and A.C. Algar. 2014. Untangling Intra- and Interspecific Effects on Body Size Clines Reveals Divergent Processes Structuring Convergent Patterns in Anolis lizards. The American Naturalist 184: 636-646.
* This pattern was measured from 16 Anolis species: nine in the sagrei clade (Cuba) and seven in the cybotes clade (Hispaniola). The finding of small body size at high elevations is the inverse expectation of Bergmann’s rule. Bergmann’s rule, as originally conceived, states that endothermic species living in colder climates should be larger (or have a larger surface area to volume ratio), all else equal, to conserve heat. As lizards are ectothermic, one would expect an inverse Bergmann. Perhaps we could call the inverse cline Nnamgerb’s rule? It does have a certain charm to it, no?
** I wonder if the authors might chime in in the comments section. What does it mean that a size-elevation cline wasn’t found on Cuba when using the mean size and elevation of each population (Fig 5 below), but it was found when species identity was ignored (Fig 1 above)? Is this an example of Simpson’s paradox?
Zookeeper Amber Carney sent these photos of what is likely Anolis carolinensis. The lizards were spotted in Balboa Park, San Diego, CA, at 3pm on the 19th of April. They’ve been reported in Los Angeles but, to the best of my and Jonathan Losos’s knowledge, never in San Diego. Has anyone else observed wild anoles in San Diego? Range expansion!
If you’re anything like me, the first image you conjure in your mind when you hear the word Jamaica is a phylogenetic tree showing a monophyletic radiation of six Anolis species representing four ecomorph classes and one unique.
What, that’s not what you thought of?
Anolis grahami, a beauty!
The anoles of Jamaica: Read all about them!
1) Anolis garmani is a crown-giant, although it’s on the small end, if you ask me.
2) Anolis grahami is a trunk-crown and gram for gram one of the prettiest anoles out there.
3) Anolis lineatopus is a trunk-ground anole with a stunningly large cream colored dewlap.
4) Anolis opalinus is a smallish trunk-crown nicely found in a Blue Mountains coffee grove.
5) Anolis reconditus is a unique anole – very little known about it (but see).
6) Anolis valencienni is a twig anole, large and at high population densities for a twig.
7) (And yes, A. sagrei is there, but it’s invaded from Cuba over historical time.)
What do diseases like Ebola, Influenza, SARS, and Rabies have in common? Well, for one, they’re all viruses. Second, and more germane to this discussion, they’re all zoonoses–diseases that are usually harbored in non-human animal hosts but occasionally spill over into humans. Zoonoses are the subject of David Quammen’s excellent and aptly named new book, Spillover.
Quammen is in peak form with Spillover: he tracks these diseases and the researchers who study them from goat farms in Holland to bat caves in Uganda to wild meat markets on the Chinese mainland near Hong Kong. The book reads like a thriller–where exactly is Ebola lurking?– but doesn’t need fictional plot twists to keep the pages turning. Quammen’s accurate, clear, and exiting descriptions of the epidemiology, ecology, and evolution of zoonotic diseases keeps the pages turning instead.
A central message of Spillover is that a “successful” zoonosis is the result of opportunity. That is to say, the life history of many zoonotic agents does not require a pass through human populations; they will survive, reproduce, and spread just fine in their animal hosts. However, if a zoonotic disease happens to find itself in a human body, those viruses (or bacteria, or protozoans, etc.) that can survive will survive, reproduce, and possibly spread to other people. Thus, the story of zoonoses is the story of humans creating the opportunity for spillover by coming into contact with animal hosts. For example, HIV (human immunodeficiency virus) is closely related to SIV (simian immunodeficiency virus) and all evidence suggests that it spilled into human populations through the use of chimpanzees for food. Nipah, a neurological and respiratory disease in Malaysia, Singapore, and Bangladesh, likely spills over into human populations through contact with fruit bat feces, contact that is becoming more common as human cities, towns, and agricultural fields encroach on the tropical rainforests that the bats call home. In sum, close contact with wild animals greatly increases the chance of spillover.
Close contact with wild animals… Close contact… Hmmm, what is it we do again?…
Situated at the northern end of the the Lesser Antillean island chain, Montserrat is home to a number of interesting herps, including the endemic galliwasp Diploglossus montisserrati, the endemic skink Mabuya montserratae, and the endemic anole Anolis lividus. This anole was bravely investigated and reported on by Anole Annals’ intrepid anoleologist Martha Munoz. If your inquiry into the reason I used the words “bravely” and “intrepid” has left you a little lost, the smoke Montserrat is emitting from its active volcano will drag you to the answer: Martha was on the island when the Soufrière Hills dome collapsed and spewed volcanic ash 9 miles skyward!
Collapse of the dome sends ash skywards. January 2010. Photo by Martha Munoz.
The Grenadines. (http://en.wikipedia.org/wiki/File:Grenadines- Archipelago)
Check out the Grenadines, a polyphyletic chain of approximately 600 islands found at the southern end of the Lesser Antilles. The islands north of the Martinique Channel are governed by St. Vincent. The islands south of the Martinique Channel are governed by Grenada. (Grenada, you’ll recall, was invaded by the US in 1983).
Given Martinique Channel’s apparent role as a political boundary, I wondered if it is also an important biogeographical boundary, much like Wallace’s Line in Indonesia. Wallace’s line, which passes through through the Lombok Strait between Bali and Lombok and between Borneo and Sulawesi, denotes a clear faunal break between Asian and Oceanic faunas. The biogeographical explanation is that Wallace’s line follows the transition from continental shelf to deep water channel, which serves as a barrier for migration.
Martinique Channel (line added).
A look at the Caribherp distribution of herpetofauna found on the Grenadines suggests that the Martinique Channel is not actually a biogeographic break. The distribution of most herps found on the Grenadines crosses the channel, suggesting that the channel is not a barrier to migration. And, consistent with this, Google Earth suggests that the channel is not very deep.
Oh, almost forgot: the Anolis species on the Grenadines are A. aeneus, A. richardi, and the invasive A. sagrei.
Anolis aeneus. Photo from http://www.kingsnake.com/westindian/anolisaeneus5.JPG.
Anolis richardi. (Photo from http://reptile-database.reptarium.cz)
Little Cayman is a quiet little diving community with less than 100 residents, made up mostly of expats and people who run the hotels that host the tourists attracted by some of the best diving and snorkeling in the Caribbean. When I was there, we met some locals who gave us a tour of the island and we circumnavigated Little Cayman in about 20 minutes by car. We saw the endangered Cyclura caymanensis on the northern side of the island, in a spot where they congregate for tourists to feed them. As far as Anolis go, Little Cayman has Anolis maynardi, a very long-snouted green anole. They also have a red-dewlapped population of Anolis sagrei that Jason Kolbe showed is more closely related to populations of A. sagrei on Cuba than they are to populations of red-dewlapped A. sagrei on Grand Cayman.
The Western arm of Grand Cayman, the biggest island, feels a little bit like South Beach in Miami, with expensive resort hotels, boutique shopping, and a rocking beach and nightlife scene. As you go farther east, you find the the classic Caribbean dry forests growing among the karst outcroppings. The endangered Grand Cayman Blue Iguana, Cyclura lewisi, has a remnant population in and around the botanical gardens on the east end of the island. This species is not blue like Anolis gorgonae but it does have a bluish-green sheen depending on how the light hits it.
The Grand Cayman Blue Iguana (photo from the Wikipedia page)
Anolis conspersus is notable on Grand Cayman – it is related to A. grahami from Jamaica but has evolved a beautiful purplish-blue dewlap, very different from A. grahami’s yellow dewlap.
Cayman Brac feels like Little Cayman, except that it is bigger, has a few population centers, and is dominated by a bluff that grows from nothing in the west to a towering 150 feet in the east. During hurricanes, people living on Cayman Brac used to climb up to and take refuge in caves that weave back into the bluff. We spent some time on Brac looking for a cryptic invasion of Anolis sagrei sagrei into the endemic Anolis sagrei luteosignifer population. That project is ongoing in the lab. It was fun to work there and we met many friendly people.
It’s common wisdom that formalin-preserved samples can’t be DNA sequenced because formalin degrades DNA beyond use . However, a paper recently appeared in Genome Research, describing successful whole genome sequencing of formalin-prepared samples.
