Anole Annals

Here at AA, we’re a bit obsessed with lizards with things on their noses, technically called “rostral appendages,” and sometimes, depending on shape, “horns.” A lot of this interest comes Anolis proboscis, the horned anole of Ecuador, about which we’ve written much before.

Almost as cool as horned anoles (really, that’s an unfair standard) is the Sri Lankan lizard genus Ceratophora, which contains three species with rostral (or nasal) appendages, and two other species that are appendage-less. In a recent paper in Journal of Zoology, Johnston et al. discuss the evolution of these appendages. It’s long been debated whether the appendages evolved independently in each species or once in the ancestral Ceratophora, followed by loss in the two nasally-naked species. By combining analyses of phylogeny (which produces somewhat inconclusive reconstructions of ancestral phenotype), morphology and allometry, the authors conclude that the appendages most likely evolved independently in each of the three species. Moreover, they suggest the blob-like appendage of C. tennenti (bottom photo) may have evolved for crypsis, but the more horn-like appendages of the other two species probably resulted from sexual selection.

While on the topic of nasal horns, I decided to see if there are any new photos of the other horned anole, A. phyllorhinus, on the web, and indeed there are. See below. The natural history of this species, which likely evolved its horn independently of A. proboscis, awaits further study.

from http://ipt.olhares.com/data/big/506/5069364.jpg

from http://www.reptarium.cz/content/photo_rd_05/Anolis-phyllorhinus-03000033975_01.jpg

The rise in number of recognized reptile species through the years.

The number of described species of reptiles has increased extraordinarily in recent times. In a fascinating recent article, Pincheira-Donoso and colleagues have catalogued this increase, as well as describing the taxonomic distribution of present-day reptile diversity. They report that since 2000, the number of described species of lizards has increased by 1164, a remarkable increase of 26%. They also point out that reptile diversity among clades is right-skewed, with most genera containing relatively few species and a few containing a lot. And, of course, they highlight everyone’s favorite genus, Anolis, as one of the largest outliers.

Speaking of anoles, AA wondered how anole diversity has changed since 2000. Daniel Pincheira-Donoso kindly provided the answer, with information provided by co-author Peter Uetz. Since 2000, 42 species have been described, bringing the total in March 2012 (when data were compiled) to 384 (the list of new species from 2000 til the present appears below). That’s only a 12% increase, lagging behind lizards in general, but more on par with the description rate for snakes, which has increased 16% over that period. As AA readers are well aware, however, new anole species are being described at a high rate (e.g., 1,2) and, indeed, Uetz’s Reptile DataBase now puts the number at 391.

What’s behind this incredible burst of species description, both in anoles and more broadly? Some of it is the result of exploration and discovery of truly new, previously unknown, lizards. But most of the increase—in my humble estimation—is the result of the taxonomic splitting of previously widespread species into multiple species. Systematics goes through phases of “lumping” and “splitting” and the field in general seems to be experiencing a massive phase of splitting at the moment. In some cases, this is the result of taxa being differentiated on the basis of morphological characters. However, most is the result of the discovery of genetic differentiation among populations. A naysayer might be prompted to say that this has gone to far, that species are sometimes being described on the basis of minor, insubstantial differentiation. It will be interesting to see if and how much the pendulum swings back.

Are these really the same species?

Regardless, one of the reasons that anole diversity has not increased as much as that in other taxa is that anole systematists—to date—have been restrained in their splitting, particularly in the West Indies. Substantial genetic diversity has been found among populations in many anole species, differentiation so great that many would have described four, six, or eight species from single widespread Caribbean taxa. This, of course, may change in the future, and the diversity of Caribbean anoles may skyrocket.

Below are the abstract of the Pincheira-Donoso paper and then the list of new anoles described from 2000-2012. And when you’re done reading those, check out Daniel Pincheira-Donoso’s website, with much information on Daniel and his work on Liolaemus.

Abstract:

Reptiles are one of the most ecologically and evolutionarily remarkable groups of living organisms, having successfully colonized most of the planet, including the oceans and some of the harshest and more environmentally unstable ecosystems on earth. Here, based on a complete dataset of all the world’s diversity of living reptiles, we analyse lineage taxonomic richness both within and among clades, at different levels of the phylogenetic hierarchy. We also analyse the historical tendencies in the descriptions of new reptile species from Linnaeus to March 2012. Although (non-avian) reptiles are the second most species-rich group of amniotes after birds, most of their diversity (96.3%) is concentrated in squamates (59% lizards, 35% snakes, and 2% amphisbaenians). In strong contrast, turtles (3.4%), crocodilians (0.3%), and tuataras (0.01%) are far less diverse. In terms of species discoveries, most turtles and crocodilians were described early, while descriptions of lizards, snakes and amphisbaenians are multimodal with respect to time. Lizard descriptions, in particular, have reached unprecedented levels during the last decade. Finally, despite such remarkably asymmetric distributions of reptile taxonomic diversity among groups, we found that the distributions of lineage richness are consistently right-skewed, with most clades (monophyletic families and genera) containing few lineages (monophyletic genera and species, respectively), while only a few have radiated greatly (notably the families Colubridae and Scincidae, and the lizard genera Anolis and Liolaemus). Therefore, such consistency in the frequency distribution of richness among clades and among phylogenetic levels suggests that the nature of reptile biodiversity is fundamentally fractal (i.e., it is scale invariant). We then compared current reptile diversity with the global reptile diversity and taxonomy known in 1980. Despite substantial differences in the taxonomies (relative to 2012), the patterns of lineage richness remain qualitatively identical, hence reinforcing our conclusions about the fractal nature of reptile biodiversity.

New Anole Species:

Anolis cusuco (MCCRANIE, KÖHLER & WILSON 2000)

Anolis kreutzi (MCCRANIE, KÖHLER & WILSON 2000)

Anolis toldo FONG & GARRIDO 2000

Anolis hobartsmithi (NIETO-MONTES DE OCA 2001)

Anolis ocelloscapularis (KÖHLER, MCCRANIE & WILSON 2001)

Anolis oporinus GARRIDO & HEDGES 2001

Anolis roatanensis (KÖHLER & MCCRANIE 2001)

Anolis terueli NAVARRO, FERNANDEZ & GARRIDO 2001

Anolis wampuensis (MCCRANIE & KÖHLER 2001)

Anolis yoroensis (MCCRANIE, NICHOLSON & KÖHLER 2001)

Anolis zeus (KÖHLER & MCCRANIE 2001)

Anolis ruibali NAVARRO & GARRIDO 2004

Anolis paravertebralis (BERNAL-CARLO & ROZE 2005)

Anolis umbrivagus (BERNAL-CARLO & ROZE 2005)

Anolis anatoloros (UGUETO, RIVAS, BARROS, SÁNCHEZ-PACHECO & GARCÍA-PÉREZ 2007)

Anolis datzorum (KÖHLER, PONCE, SUNYER & BATISTA 2007)

Anolis gruuo (KÖHLER, PONCE, SUNYER & BATISTA 2007)

Anolis kunayalae (HULEBAK, POE, IBÁNEZ & WILLIAMS 2007)

Anolis magnaphallus (POE & IBÁNEZ 2007)

Anolis pseudokemptoni (KÖHLER, PONCE, SUNYER & BATISTA 2007)

Anolis pseudopachypus (KÖHLER, PONCE, SUNYER & BATISTA 2007)

Anolis williamsmittermeierorum POE & YAÑEZ-MIRANDA 2007

Anolis apletophallus (KÖHLER & SUNYER 2008)

Anolis campbelli (KÖHLER & SMITH 2008)

Anolis cryptolimifrons (KÖHLER & SUNYER 2008)

Anolis cuscoensis (POE, YAÑEZ-MIRANDA & LEHR 2008)

Anolis soinii (POE & YAÑEZ-MIRANDA 2008)

Anolis anchicayae (POE, VELASCO, MIYATA & WILLIAMS 2009)

Anolis ibanezi (POE, LATELLA, RYAN & SCHAAD 2009)

Anolis lyra (POE, VELASCO, MIYATA & WILLIAMS 2009)

Anolis monteverde (KÖHLER 2009)

Anolis morazani (TOWNSEND & WILSON 2009)

Anolis anoriensis (VELASCO, GUTIÉRREZ-CÁRDENAS & QUINTERO-ANGEL 2010) Anolis charlesmyersi (KÖHLER 2010)

Anolis osa (KÖHLER, DEHLING & KÖHLER 2010)

Anolis otongae (AYALA-VARELA & VELASCO 2010)

Anolis podocarpus (AYALA-VARELA & TORRES-CARVAJAL 2010)

Anolis unilobatus (KÖHLER & VESELY 2010)

Anolis benedikti (LOTZKAT, BIENENTREU, HERTZ & KÖHLER 2011)

Anolis tenorioensis (KÖHLER 2011)

Anolis sierramaestrae (HOLÁŇOVÁ, REHÁK & FRYNTA 2012)

Anolis ginaelisae (LOTZKAT, HERTZ, BIENENTREU & KÖHLER 2013)

Academic conferences are important venues for researchers to learn what is new and exciting in science and to present our more recent work. The annual meetings for the Society of Integrative and Comparative Biology (SICB) is one major conference drawing over 2,000 scientists from around the world. This conference is always held in January and usually features an embarrassment of anoles. The 2012 SICB conference in Charleston, South Carolina featured many interesting talks on anoles, ranging from discussions on new eve-devo resources in this emerging model system to studies of behavioral ecology and thermal physiology (1, 2). SICB 2013 was recently held in San Francisco, and those of us following research in Anolis lizards had plenty to see and learn as there were 18 talks and posters featuring anoles. I attended many of these and summarized the findings as best I could in several AA posts this past January (1, 2, 3, 4).

As it turns out, SICB is not the only conference where anole biologists congregate in large numbers. Another major venue for learning what’s new in Anolis research is the joint meeting of the Society for Systematic Biology (SSB), Society for the Study of Evolution (SSE), and the American Society of Naturalists (ASN). This meeting is generally referred to as the Evolution conference, for short.

This year the Evolution conference will be held in Snowbird, Utah in the last week of June. Two days ago the organizers released the online program for the conference. A quick search using “Anolis” or “anole” as keywords revealed seven talks about these lizards. I’ll be attending this conference (and speaking!), and I’ll be getting updates on each of these studies onto the Anole Annals as much as I can, so stay tuned for more! In the meanwhile, here are titles for all the talks I found about Anolis. If there are more out there that I missed, please let me know!

(1) Title: Natural selection, developmental trajectories, and quantitative genetics underlying intraspecific variation in sexual dimorphism in an island lizard.
Authors: Cox, Robert; Daugherty, Christopher; Price, Jennifer; McGlothlin, Joel.

(2) Title: Extreme sex differences in the development of body size and sexual signals are mediated by hormonal pleiotropy in a dimorphic lizard.
Authors: Cox, Christian L.; Hanninen , Amanda F; Cox, Robert M.

(3) Title: Genomics of local adaptation and colorful pigmentation in Anolis lizards.
Authors: Crawford, Nicholas; McGreevy, Jr., Thomas; Mullen, Sean; Schneider, Christopher.

(4) Title: Identification of sex specific molecular markers from reduced-representation genome sequencing.
Authors: Gamble, Tony; Zarkower, David.

(5) Title: Natural selection on the thermal performance curve of Anolis sagrei.
Authors: Logan, Michael L; Cox, Robert M; Calsbeek, Ryan G.

(6) Title: Testing for simultaneous divergence and gene flow in sister-pairs of physiologically divergent Anolis lizards from Puerto Rico.
Author: McElroy, Matthew.

(7) Title: Divergence in coloration and the evolution of reproductive isolation in the Anolis marmoratus species complex.
Authors: Muñoz, Martha; Crawford, Nicholas; McGreevy, Jr., Thomas; Schneider, Christopher.

Fig. 1 from Muñoz et al. (2013) Anolis marmoratus subspecies on Basse Terre (left) and Grande Terre (right)

Unlike the extensive within-island speciation that anoles have undergone in the Greater Antilles, we have no evidence that the same has occurred in the Lesser Antilles. Rather, Lesser Antillean islands that contain two species are thought to be the result of dispersal events rather than in situ cladogenesis. Despite such low species diversity, however, phenotypic diversity on many of these islands certainly is not lacking. Some Lesser Antillean anoles exhibit spectacular geographic variation in head, body and dewlap colouration and pattern, as well as body size and scalation, that appears to be adaptive to different environments. So, while this variation has not led to complete speciation in any Lesser Antillean anole, is there some evidence that these phenotypically divergent populations are at some stage of the speciation process? Also, how does phenotypic divergence occur on these smaller islands when there seems to be little opportunity for geographical isolation?

AA contributor, Martha Muñoz and colleagues tackle these very questions in a recent paper in Molecular Ecology. Muñoz et al. focus on the stunning phenotypic diversity of the Anolis marmoratus complex on Guadeloupe, which has been categorised into 12 subspecies. On Grande Terre, in particular, two subspecies can be found: A. m. speciosus inhabits mesic habitats in the southwest and A. m. inornatus inhabits the xeric lowlands of the north and east. Males share a yellow-orange coloured dewlap but differ in head, body and eye ring colouration, while females and juveniles of the two subspecies are similarly drab in colour. Continue reading →

Seaweed washed ashore on a Bahamian island. Photo by Dave Spiller.

Ecologists are increasingly recognizing the myriad connections not only among species within an ecosystem, but between species in different ecosystems. Case in point: seaweed often washes ashore, and it affects leaves on the plants found near the shoreline. How’s that, you might ask? Well, the seaweed decays and releases nutrients that act as fertilizer, increasing the growth of land plants. That’s good for the plants, but it also makes their leaves more tasty, and hence plant-eating insects are attracted and cause more damage to the leaves.

That seems straightforward enough, but then it gets more complicated. As the seaweed decays, it attracts lots of insects. And the insects, in turn, attract lizards. And, in fact, if you happen to be studying this process on small islands in the Bahamas, as Jonah Piovia-Scott and a team from UC-Davis were, then those lizards are our favorites, brown anoles. And if there are more brown anoles around, then they’ll eat more of the herbivorous insects that plague the land plants, and so the washed-up seaweed actually decrease the damage to land plant leaves, thanks to the helpful consumption of the anoles.

Except…maybe the lizards will be so delighted by the seaweed that they’ll spend all of their time there, eating the insects on the seaweed, and thus neglecting the insects on the landplants, so now the effect of seaweed on the land plants becomes negative again.

So which is it? That’s what Piovia-Scott et al. set out to discover, and they’ve just reported the results in a paper in Oecologia. And the diagram to the left explains it succinctly. Seaweed increases nitrogen in the leaves, which increases herbivory. Seaweed also increases lizard density, which decreases herbivory, though the negative effect isn’t as great as the positive effect of the nitrogen. Moreover, seaweed also causes lizards to shift their diet, which has a small (and statistically non-significant) positive effect on herbivory because the lizards aren’t eating as many of the land plant herbivores. Bottom line: seaweed increases leaf damage; lizards can’t prevent it, in part because their effects are schizophrenic: more lizards, but eating fewer herbivores.

Interestingly, these results are opposite of what the same team of authors found in a study we discussed two years ago. The difference was that in that study, a big pile of seaweed was laid out at one time and the results were followed over a short period, whereas this study followed natural seaweed deposition and compared sites differing in the amount of seaweed washed ashore, following their sites for a lengthier period of time.

One last point: how did the researchers document that the lizards were switching diet? Not from sitting around and watching the lizards, but by measuring the carbon isotope ratios in their tails. Marine vegetation tends to have higher ratios of Carbon-13 than terrestrial sources, and so insects feeding on plants from different areas will, in turn, have different ratios, which means that, in turn, one can look at the Carbon-13 ratios in lizard tissue and get a sense of from which ecosystem they’re deriving their carbon. And in this case, the more seaweed, the higher the ratio. Pretty nifty!

Anolis ginaelisae

Six large anoles of the Dactyloa clade occur in western Panama. In their explorations, Lotzkat and colleagues have collected all of them, and have just published a paper in Zootaxa reviewing these species. Their phylogenetic analyses based both on DNA and morphological characters confirm the existence of the six taxa, but also find geographically-oriented genetic differentiation in two species. In combination with morphological data, the authors split A. microtus into two species, the new one under the name A. ginaelisae.

The paper includes a nice review of all the species including spiffy color plates (see A. ibanezi below as an example) and natural history notes (short take: they’re all arboreal and almost all individuals have been caught at night). A key is also included.

Anolis ibanezi

One last note. The derivation of the new specific epithet gianaelisae is touching: ”Sebastian Lotzkat dedicates this exceptionally beautiful new species to his even more enchanting fiancée Gina Elisa Moog, who has made more than a third of his life worthwhile by now, in deepest gratitude for that wonderful time and pleasant anticipation of a mutual future.”

Abstract: “Six species of giant alpha anoles of the genus Dactyloa are known to occur in western Panama: Dactyloa casildae, D. frenata, D. ibanezi, D. insignis, D. kunayalae, and D. microtus. Based on own material collected along the highlands in Bocas del Toro, Chiriquí, and Veraguas provinces and the Comarca Ngöbe-Buglé of western Panama, we review their variation in morphological characters and the 16S rRNA mitochondrial gene. Our results support all six nominal taxa, but reveal considerable genetic differentiation between populations of the two highland species, D. casildae and D. microtus, respectively, from different localities. Correlated morphological differences confirm the existence of a cryptic species among populations currently assigned to D. microtus, which we describe as Dactyloa ginaelisae sp. nov. We provide point distribution maps, morphology and color descriptions, photographs in life, conservation status assessments, and an identification key for all seven species.”