The primary focus of the Losos Lab is on the behavioral and evolutionary ecology of lizards. Major questions concern how lizards interact with their environment and how lizard clades have diversified evolutionary. Addressing such questions requires integration of behavioral, ecological, functional morphological, and phylogenetic studies. A major focus has been the evolutionary radiation of Caribbean Anolis lizards, but other lizard radiations are also being studied. A second focus is population dynamics and behavioral ecology of local populations of the collared lizard, Crotaphytus collaris.
Anolis
Anolis is the largest amniote genus with approximately 400 described species. Nearly 150 of these species occur in the Caribbean. Two patterns of interest occur on the islands of the Greater Antilles (Cuba, Hispaniola, Jamaica, and Puerto Rico). First, on any of these islands, anoles are often extremely abundant. At any given spot, one can often easily find 4-6 species (the maximum is 11 at Soroa, Cuba). These species occupy different microhabitats (e.g., one lives on twigs in the trees, another in the grass, a third on tree trunk near the ground, and each is morphologically and behaviorally different. For example, twig anoles tend to be slender with short legs and tails, whereas the trunk-ground anoles are stocky, with long legs and poorly developed toepads. In all, six such habitat specialists are recognized, termed "ecomorphs" and named for the part of the habitat they occupy.
Most strikingly, when one goes to different islands among the Greater Antilles, one sees essentially the same set of ecomorphs on each island (with several exceptions). For example, if one saw a twig anole on Puerto Rico, one could go to each of the other islands and see a very similar looking animal living in the same sort of habitat and behaving similarly. For the most part, this is true for each of the ecomorphs.
This raises a number of questions. First, have these ecomorphs evolved independently on each island, or have they each evolved only once and someone come to occupy each island? Phylogenetic studies using mitochondrial DNA, conducted by Todd Jackman, in collaboration with Allan Larson and Kevin de Queiroz of the Smithsonian's National Museum of Natural History, clearly indicate that members of the same ecomorph class on different islands are not closely related. Hence, the similar assemblages on each island are the result of convergent evolution. Although such a phenomenon has been suggested in the past for other groups, it has never previously been demonstrated phylogenetically.
Given that species on different islands have evolved similar morphologies to live in similar habitats, the obvious hypothesis is that the morphologies reflect adaptations to those habitats. However, to understand why a particular feature is adaptive in a particular microhabitat (e.g., why short limbs should evolve in twig species), we need to know what consequences differences in morphology have for these lizards and whether such functional differences are relevant to lizards in nature. To answer the former question, we bring lizards into the lab and measure their functional capabilities in ecologically relevant ways, such as maximum sprinting, jumping, and clinging capabilities. These studies, many of which were conducted by Duncan Irschick, indicate that differences in limb length result in differences in sprinting and clinging capabilities. Similarly, differences in toe pad dimensions are related to clinging ability. Moreover, it turns out that the relationship between morphology and performance ability is context-dependent; for example, long legs confer enhanced sprinting ability on broad, but not narrow surfaces.
Field studies are then necessary to assess whether these functional differences make any difference to the organisms. Not surprisingly, they do. Species in different habitats use different surfaces and move in different ways. In escaping predators, lizards make use of their maximal sprinting capabilities. Moreover, it appears that species are adapted to perform best in the environment and with the lifestyle (foraging behavior, escape strategy, etc.) they utilize. Nonetheless, not all performance abilities are taken advantage of: for example, lizards rarely use their maximal jumping capabilities. Much of this field work was also conducted by Duncan Irschick.
An unexpected finding is that habitat specialists are convergent not only
in morphology and behavior, but also degree of sexual dimorphism.
This indicates that the ecomorph phenomenon is much more pervasive than
simply reflecting adaptations to different modes of locomotion. Most
likely, patterns of territoriality and sexual selection are also involved.
Marguerite Butler's thesis focused on the
interaction of sexual differentiation and adaptive radiation.
Probably as a result of their high population densities, anoles have a rich repertoire of signals used in many contexts. The diversity of dewlap coloration and signalling patterns is probably primarily a means of communicating intraspecifically, but also serves the purpose of species-identification. An interesting hypothesis is that the existence of these visual signals has facilitated speciation and may play a role in the extensive radiation of the genus. In addition, most anole workers have noted that anoles will display to humans. However, this behavior has been generally disregarded. However, Manuel Leal thought that maybe this represented more than the stupidity of lizards. He has demonstrated that anoles actually can fight off a snake predator by biting and not letting go. Moreover, the greater the endurance capacity of an anole (measured on lizard raceways), the greater the intensity of their displays. Hence, this may be a demonstration that anole displays toward predators are honest signals of a lizard's ability to fight off predators.
Long-term studies of anoles have been conducted on small Bahamian islands for a number of years in collaboration with Dr. David Spiller of the University of California, Davis. These studies have established that two lizards interact ecologically, perhaps by competition or intra-guild predation. In addition, these studies have explored the role that lizards play as top predators on lower levels of the food web. The nature of these experiments was radically altered in 1996 when Hurricane Lili passed directly over the islands, wiping out most populations. Now we are studying how the island ecosystems recover.
Previous studies of populations elsewhere in the Bahamas that had been
introduced 20 years previously indicated that the populations differed
in hindlimb length in a way that made sense: populations that perched on
broader surfaces had longer hindlimbs than populations on narrower surfaces.
Given that this matched the trend, seen to a much greater extent, among
the Greater Antillean ecomorphs, this suggested the hypothesis that the
populations had differentiated genetically as a result of selection in
different environments. Although this change would be rapid (15-30
lizard generations), the actual magnitude of difference among populations
was not huge (in fact, most people would not be able to detect the difference
if shown lizards from different populations). However, another alternative
is that lizards growing in different environments grow different length
legs. To test this hypothesis, we raised baby anoles on two different
surfaces at the St. Louis Zoo--either on 2x4's or on narrow (1/4") dowels.
At the end of three months, the lizards raised on broader surfaces had
longer limbs than the lizards on narrower surfaces! This suggests
that the results observed in the field may be the result of a phenotypic
plasticity in limb growth, rather than genetic differentiation. To
test this hypothesis, we plan common garden experiments in which we will
raise lizards from different islands in similar environments to see if
differences in limb length persist. Adaptive phenotypic plasticity
has never previously been documented for vertebrate hindlimbs. These
findings suggest the intriguing possibility that phenotypic plasticity
may play an important role in adaptive differentiation by permitting lizards
to occupy different habitats; once subsequent mutations arise, these differences
can then be elaborated upon by natural selection.
Diversification in Other Lizard Clades
A broadly similar approach is being taken to study the ecology and evolutionary diversification of other lizard groups. Preliminary studies, in collaboration with Dr. le Fras Mouton of the University of Stellenbosch, have investigated the extent of morphological, behavioral, and ecological diversity in cordylid lizards, a relatively unstudied family of lizards endemic to southern Africa. This group is interesting because it is not rich in species or genera (4 and 40, respectively); nonetheless, it is quite diverse ecologically and morphologically, ranging from heavily armored and stocky lizards such as Cordylus giganteus and C. cataphractus, to agile lizards so flat they look like they have been stepped upon (Platysaurus), to species that are nearly limbless and essentially function as snakes (Chamaesaura).
Other groups being studied in the lab include: life history evolution
in monitor lizards, which range in size from 15 grams to 150 kg (Dave
Pepin); Liolaemus, a South American lizard genus with approximately
150 species which shows great diversity in morphology, habitat use, and
life history (Jim Schulte); community ecology of southwestern lizards,
focusing on the behavioral consequences of morphological differences in
the highly diverse lizards faunas of the southwestern deserts (Jane
Melville); and the evolution of ontogenetic color change in snakes
(Doug Creer). All of these studies combine
phylogenetic and field approaches.
Crotaphytus
Collared lizards are generally thought of as southwestern lizards. However, approximately 8,000 years ago, hotter and drier climate allowed collared lizards to migrate into Missouri. About 3,000 years ago, the climate became wetter and cooler, as it is today, and most areas became unsuitable to collared lizards. However, habitats called "glades" occur on rocky, poor soils where forest generally does not become established. Glades with a southwestern exposure tend to be hot enough and open enough for collared lizard populations to persist. Unfortunately, many glades and their occupants are threatened by fire suppression, which allows the eastern cedar to become established. Once a canopy develops, other trees can come in, and many glade inhabitants, such as collared lizards, disappear.
Most glades today are small and isolated. As such, they are in jeopardy due to stochastic and genetic factors. Because small, peripherally-located, populations are of interest both to evolutionary and conservation biologists, we have established long-term studies on several glades within two hours' drive from campus. One glade has been studied since 1993; seven others since 1995 or 1996. On each glade, each lizard is individually identified. Because collared lizards rarely live more than four years in Missouri, we now know the life history of each lizard on the glade--when it was born, where it lived, who it's range overlapped with. Our goals are to understand change in population dynamics and genetic constitution as a consequence of individual histories. The development of microsatellite loci hopefully will allow us to establish parentage and thus permit tracing change in genetic variation as the result of the reproductive success (or lack thereof) of particular individuals. Delbert Hutchison has taken the lead in much of this work in recent years and all of the molecular work, conducted in the laboratory of Dr. Alan Templeton. John Parks has also been responsible for much of the work on many of the glades. Danielle Glossip, in her time both as an undergraduate and as a technician, was instrumental in getting these studies going.
A number of behavioral studies have been conducted. The most extensive are John Parks' studies of the effect of habitat visibility on territorial behavior and Amy Angert's study of interactions between collared lizards and fence lizards, which also occur on glades.