The parasites of Anolis lizards in the northern Lesser Antilles

Summary The helminth communities from ten species of lizard on seven islands in the Caribbean were sampled by collecting one hundred specimens of each species. Nine genera of parasites were identified; these included six nematodes, two digeneans and an acanthocephalan. No relationship was discernible between parasite density or abundance and island area or altitude, although dry islands tend to have fewer species of parasites. Anolis lizards of the bimaculatus and wattsi series share similar parasites with four out of nine species common to both series. The parasite community of lizards on these islands is depauperate with respect to similar surveys on the larger islands of the Greater Antilles.On three of the islands lizards were sub-sampled by collecting from moist woodland and more xeric habitats. These data suggest that differences between habitats are as significant as differences between islands in determining parasite burdens. Worm burdens of the commonest parasite species, T. cubensis, increased monotonically with host body size and no evidence was found to suggest that these parasites affect either host survival or fecundity. The sex-ratio of this species correlated with mean abundance of the parasite, with females the dominant sex on islands or in habitats where the parasite was common. This pattern may reflect haplodiploid sexual determination in this species.     

Phylogeography of Caribbean lizard malaria: tracing the history of vector‐borne parasites

The Anolis lizards of the eastern Caribbean islands are parasitized by several species of malaria parasites (Plasmodium). Here I focus on two species of Plasmodium, using molecular data (mitochondrial cytochrome b sequences) to recover the phylogeography of the parasites throughout the Lesser Antilles and Puerto Rico. The two parasites were originally described as a single species, P. azurophilum, which infects both red and white blood cells. Here the two species are termed P. azurophilum Red and P. azurophilum White based on their host cell type. Six haplotypes were found in 100 infections sequenced of P. azurophilum Red and six in 45 infections of P. azurophilum White. Nested clade analysis revealed a significant association of geographical location and clades as well as a pattern of past fragmentation of parasite populations. This is consistent with the hypothesis that vector‐borne parasites such as malaria may be subject to frequent local extinctions and recolonizations. Comparison of the phylogeography of the lizard and parasites shows only weak concordance; that is, the parasites colonized the lizards in the islands, but dispersal events between islands via vectors or failed lizard colonizations were present. The two parasites had different histories, P. azurophilum Red colonized the islands from both the north and south, and P. azurophilum White originated in the central Lesser Antilles, probably from P. azurophilum Red, then moved to both north and south. This is the first study to examine the biogeography of a pair of sibling species of vector‐borne parasites within an island archipelago system.     

Progress Towards the Eradication of Amblyomma variegatum from the Caribbean

Progress in the Caribbean Amblyomma Program (CAP) is reviewed since its inception in 1995 when regional eradication activities for Amblyomma variegatum ticks were initiated using Bayticol pour-on. Technical achievements in the various islands were slow initially, and showed a wide diversity in attaining eradication targets. St. Kitts, considered as a model program, eliminated the tropical Bont tick (TBT) from most of the island in less than 3 years. However, the elimination of very low numbers of residual adult TBT that persisted in three ‘hot-spots’ took another 3 years. A similar problem was faced in St. Lucia, although the approach there was to cull the wild cattle in the last remaining hot-spot. Both islands were certified as ‘Provisionally free from TBT’ in November 2001. In 2002, Anguilla and Montserrat attained the same status, and Barbados and Dominica also qualify for certification. Certification is based on strict, three-monthly, surveillance criteria: essentially, two successive TBT-free surveillance rounds on a statistically acceptable sample of the livestock population. Within the responsibility of the CAP, three islands remain TBT-infested, Antigua, Nevis, and St. Martin/St. Maarten. Nevis is of concern because it has been operational since late 1995, and appears unable to resolve the problem of treating stray small ruminants. Current funding should be adequate to complete eradication on Nevis and in St. Martin/St. Maarten. The major outstanding challenge is Antigua. In comparison to other islands they have the largest number of livestock, and have much larger populations than originally reported: sheep and goats are 4–5-fold higher, and cattle are 1.35-fold higher. The cost for Bayticol is, therefore, almost double and an additional US$ 1.5 million is required for that commodity alone. This revised version was published online in July 2006 with corrections to the Cover Date.     

Patterns of ecomorphological convergence among mainland and island Anolis lizards

Differing selective pressures on islands versus the mainland may produce alternative evolutionary outcomes among closely related lineages. Conversely, lineages may be constrained to produce similar outcomes in different mainland and island environments, or mainland and island environments may not differ significantly. Among the best‐studied island radiations are Caribbean Anolis lizards. Distinct morphotypes, or ‘ecomorphs’, have been described, and the same ecomorphs have evolved independently on each Greater Antillean island. The mainland Anolis radiation has received much less attention. We use a large morphological data set and a novel phylogenetic hypothesis to show that mainland Anolis did not evolve the same morphotypes as island Anolis, despite some island species being more closely related to mainland species than to island species that share their morphotype. A maximum of four of the six Caribbean ecomorphs were found to exist on the mainland, and just 15 of 123 mainland species are assignable to a Caribbean ecomorph. This result was insensitive to differing taxon samples and alternative phylogenetic hypotheses. Mainland convergence to a Caribbean ecomorph occurs only among species assigned to the grass‐bush ecomorph. Thus, the ecomorphs that have evolved convergently multiple times in the Caribbean have not evolved in parallel on the mainland. These results are consistent with the hypothesis that mainland and island environments offer different selective pressures. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 852–859.     

Host specificity shapes population structure of pinworm parasites in Caribbean reptiles

Host specificity is one of the potential factors affecting parasite diversification because gene flow may be facilitated or constrained by the number of host species that a parasite can exploit. We test this hypothesis using a costructure approach, comparing two sympatric pinworm parasites that differ in host specificity – Parapharyngodon cubensis and Spauligodon anolis – on the Puerto Rican Bank and St. Croix in the Caribbean. Spauligodon anolis specializes on Anolis lizards, whereas P. cubensis parasitizes Anolis lizards as well as many other species of lizards and snakes. We collected lizards from across the Puerto Rican Bank and St. Croix, sampled them for S. anolis and P. cubensis and generated nuclear and mitochondrial sequence data from the parasites. We used these data to show that P. cubensis is comprised of multiple cryptic species that exhibit limited population structure relative to S. anolis, which is consistent with our prediction based on their host specificity. We also provide evidence that the distribution of P. cubensis species is maintained by competitive exclusion, and in contrast to previous theoretical work, the parasites with the greatest number of host species also reach the highest prevalence rates. Overall, our results are consistent with the hypothesis that host specificity shapes parasite diversification, and suggest that even moderate differences in host specificity may contribute to substantial differences in diversification.     

Species concepts and malaria parasites: detecting a cryptic species of Plasmodium.

Species of malaria parasite (phylum Apicomplexa: genus Plasmodium) have traditionally been described using the similarity species concept (based primarily on differences in morphological or life-history characteristics). The biological species concept (reproductive isolation) and phylogenetic species concept (based on monophyly) have not been used before in defining species of Plasmodium. Plasmodium azurophilum, described from Anolis lizards in the eastern Caribbean, is actually a two-species cryptic complex. The parasites were studied from eight islands, from Puerto Rico in the north to Grenada in the south. Morphology of the two species is very similar (differences are indistinguishable to the eye), but one infects only erythrocytes and the other only white blood cells. Molecular data for the cytochrome b gene reveal that the two forms are reproductively isolated; distinct haplotypes are present on each island and are never shared between the erythrocyte-infecting and leucocyte-infecting species. Each forms a monophyletic lineage indicating that they diverged before becoming established in the anoles of the eastern Caribbean. This comparison of the similarity, biological and phylogenetic species concepts for malaria parasites reveals the limited value of using only similarity measures in defining protozoan species.     

ADAPTATION AND CONSTRAINT IN THE EVOLUTION OF SPECIALIZATION OF BAHAMIAN ANOLIS LIZARDS

Interspecific interactions affect habitat use and subsequent morphological adaptation in Anolis lizards. We examined populations of two species of Anolis lizards that evolved in the species-rich communities of Cuba and are now widespread in the Bahamas. Because the species occupy islands in the Bahamas that vary in the number of lizard species present and other characteristics, we predicted that directional selection should have led to morphological differentiation. In particular, we expected that populations on one-species islands should have evolved toward a generalist morphology because of the lack of competitors. Divergence in both species has been adaptive; populations that use wider perches have longer legs. Nonetheless, these differences are relatively minor, and none of the populations appears to have differentiated from its ancestral “ecomorph” type toward a more generalized morphology. This stasis mirrors a trend observed in the radiation of Caribbean anoles, which exhibits repeated instances of evolutionary specialization, but few or no cases of reversion to a more generalized condition. The explanation for this directionality of evolution is not obvious but probably involves the tendency of specialized species to continue using and further adapting the niches for which they are specialized even as conditions change.     

Phylogeography of the endemic St. Lucia whiptail lizard Cnemidophorus vanzoi: Conservation genetics at the species boundary

Vicariance and isolation leading to speciation of reptiles on islands is well exemplified in a number of taxa in the Caribbean. The St. Lucia whiptail (Cnemidophorus vanzoi), considered a single species, is found on two small islets (Maria Major and Maria Minor) off the main island of St. Lucia. From lizards collected from both localities, we gathered morphological measurements and analysed the genetic divergence between populations, using a molecular survey of ∼ ∼2800 mtDNA base pairs and 8 microsatellites. There are significant differences in body size and general form and fixed but small mtDNA differences between island populations. Microsatellites reveal low diversity within populations but very high differentiation between islands with non-overlapping allele size ranges at all except one microsatellite and two loci exhibiting single-base polymorphism, fixed between islands. Based on these results, we examine published criteria to determine whether the studied island forms could be considered true species. According to the phylogenetic species concept and Moritz’s evolutionary significant unit (ESU) criteria, the two lizard populations can be considered separate entities. Crandall et al.’s (2000, Trends Ecol. Evol., 15, 290–295) broader categorization of population distinctiveness, based on concepts of ecological and genetic exchangeability, produces conflicting results depending on the interpretation of the observed ecological data. Following Fraser and Bernatchez’s (2001, Mol. Ecol., 10, 2741–2752) framework for management decisions when ecological data are not sufficient we propose that the lizard populations on the Maria islands are on differing evolutionary trajectories and thus at the species boundary. The populations are of high priority to conservation, thus meriting separate management.     

Expanding the understanding of local community assembly in adaptive radiations

Communities are thought to be assembled by two types of filters: by the environment relating to the fundamental niche and by biotic interactions relating to the realized niche. Both filters include parameters related to functional traits and their variation along environmental gradients. Here, we infer the general importance of environmental filtering of a functional trait determining local community assembly within insular adaptive radiations on the example of Caribbean Anolis lizards. We constructed maps for the probability of presence of Anolis ecomorphs (ecology‐morphology‐behavior specialists) on the Greater Antilles and overlaid these to estimate ecomorph community completeness (ECC) over the landscape. We then tested for differences in environmental parameter spaces among islands for real and cross‐fitted ECC values to see whether the underlying assembly filters are deterministic (i.e., similar among islands). We then compared information‐theoretic models of climatic and landscape parameters among Greater Antillean islands and inferred whether body mass as functional trait determines ECC. We found areas with high ECC to be strongly correlated with environmental filters, partly related to elevation. The environmental parameters influencing high ECC differed among islands. With the exception of the Jamaican twig ecomorph (which we suspect to be misclassified), smaller ecomorphs were more restricted to higher elevations than larger ones which might reflect filtering on the basis of differential physiological restrictions of ecomorphs. Our results in Anolis show that local community assembly within adaptive island radiations of animals can be determined by environmental filtering of functional traits, independently from species composition and realized environmental niche space.     

A Geographic Mosaic of Plant–Pollinator Interactions in the Eastern Caribbean Islands

The interplay between generalized and specialized plant–animal interactions is a core concept in understanding the evolution of mutualisms. Within the Eastern Caribbean, Heliconia bihai is a dominant forest species in the southern island of St. Vincent where H. caribaea is virtually absent. Heliconia caribaea is most common on the northern island of St. Kitts where H. bihai is restricted to the tops of the highest peaks. Both species are abundant on the central island of Dominica. We compared flowering patterns, nectar characteristics, and visitation frequency of hummingbirds in the two heliconias on the three islands to determine the extent of geographic variations in this plant–pollinator mutualism. The peak flowering season of the two heliconias was observed to be in April–May on all three islands with little within‐ and between‐island variations. Nectar production significantly varied between species and between islands. Visitation patterns by the principal hummingbird pollinators also varied between the islands: (1) on Dominica, only females of a single species of hummingbird pollinated the flowers of H. bihai (sexual specialization), whereas both sexes of the same hummingbird pollinated the flowers of H. caribaea (species specialization); (2) on St. Vincent, both sexes of the same hummingbird pollinated the flowers of H. bihai (species specialization); and (3) on St. Kitts, only females pollinated the flowers of H. bihai (sexual specialization), whereas several species of hummingbird visited the flowers of H. caribaea (species generalization). We propose that the Heliconia–hummingbird interactions in the Eastern Caribbean represent a geographically variable coevolutionary mosaic of plant–pollinator interactions.     

Habitat partitioning and morphological differentiation: the Southeast Asian Draco lizards and Caribbean Anolis lizards compared

Sympatric species that initially overlap in resource use are expected to partition the environment in ways that will minimize interspecific competition. This shift in resource use can in turn prompt evolutionary changes in morphology. A classic example of habitat partitioning and morphological differentiation are the Caribbean Anolis lizards. Less well studied, but nevertheless striking analogues to the Anolis are the Southeast Asian Draco lizards. Draco and Anolis have evolved independently of each other for at least 80 million years. Their comparison subsequently offers a special opportunity to examine mechanisms of phenotypic differentiation between two ecologically diverse, but phylogenetically distinct groups. We tested whether Draco shared ecological axes of differentiation with Anolis (e.g., habitat use), whether this differentiation reflected interspecific competition, and to what extent adaptive change in morphology has occurred along these ecological axes. Using existing data on Anolis, we compared the habitat use and morphology of Draco in a field study of allopatric and sympatric species on the Malay Peninsula, Borneo and in the Philippines. Sympatric Draco lizards partitioned the environment along common resource axes to the Anolis lizards, especially in perch use. Furthermore, the morphology of Draco was correlated with perch use in the same way as it was in Anolis: species that used wider perches exhibited longer limb lengths. These results provide an important illustration of how interspecific competition can occur along common ecological axes in different animal groups, and how natural selection along these axes can generate the same type of adaptive change in morphology.     

Distribution anomalies in avian haemosporidian parasites in the southern Lesser Antilles

We compared the haemosporidian parasite faunas (Plasmodium and Haemoproteus) of small land birds on the islands of St Lucia, St Vincent and Grenada in the southern Lesser Antilles. The islands differ in distance from the South American source of colonists, proximity to each other, and similarity of their avifaunas. On each island, we obtained 419–572 blood samples from 22–25 of the 34–41 resident species. We detected parasite infection by PCR and identified parasite lineages by sequencing a portion of the mitochondrial cytochrome b gene. Parasite prevalence varied from 31% on St Lucia to 22% on St Vincent and 18% on Grenada. Abundant parasite lineages differed between the three islands in spite of the similarity in host species. As in other studies, the geographic distributions of the individual parasite lineages varied widely between local endemism and broad distribution within the West Indies, including cases of long‐distance disjunction. St Vincent was unusual in the near absence of Plasmodium parasites, which accorded with low numbers of suitable mosquito vectors reported from the island. Parasites on St Vincent also tended to be host specialists compared to those on St Lucia and Grenada. Similarity in parasite assemblages among the three islands varied in parallel with host assemblage similarity (but not similarity of infected hosts) and with geographic proximity. Parasite prevalence increased with host abundance on both St Lucia and St Vincent, but not on Grenada; prevalence did not vary between endemic and more widespread host species. In addition, the endemic host species harbored parasites that were recovered from a variety of non‐endemic species as well. These results support the individualistic nature of haemosporidian parasite assemblages in evolutionarily independent host populations.     

Parasites and the evolution of extravagant male characters: Anolis lizards on Caribbean islands as a test of the Hamilton-Zuk hypothesis

Anolis lizards from Puerto Rico (five species from one site), Curaçao and Aruba in the southern Caribbean (2 populations), and 22 populations from 14 islands in the eastern Caribbean were surveyed for blood parasites (two species of Plasmodium and haemogregarines). Literature records for gut helminths from nine of these populations were added to the data set. Dorsal body color and dewlap color of males were also observed and classified into objective classes with no subjective view of showiness. These data were used to test the among-species prediction of the Hamilton-Zuk hypothesis which states that species harboring more harmful parasites over their evolutionary history will be more likely to evolve extravagant sexually dimorphic traits. Critics have noted important shortcomings in previous tests of the prediction; here we corrected for these errors. Parasite loads (prevalence and number of species) and dorsal and dewlap color varied substantially among the populations sampled. However, there was no association of parasite load with color either in a broad analysis or when correcting for phylogenetic relationships among the lizard species.     

Revealing the geographic origin of an invasive lizard: the problem of native population genetic diversity

The brown anole, Anolis sagrei, is one of the most widespread and successful colonisers of the diverse Anolis genus, which comprises c. 400 species occurring naturally in Central and South America and the Caribbean. Based on extensive between and within population sampling from a previously published study (334 mitochondrial DNA sequences) and sampling for this study (37 mtDNA sequences), we reconstruct a phylogeny and produce a haplotype network to assign a recently introduced population in St Vincent, Lesser Antilles to its geographic origin. A single haplotype was present in the St Vincent population, which was identical to a haplotype from Tampa, FL. We show that genetic diversity within native range populations, combined with low frequencies of introduced haplotypes in native ranges, may impair attempts to identify source populations, even despite intensive sampling effort. The absence of mtDNA haplotype diversity suggests a significant genetic founder effect within the St Vincent population.     

St Lucia Whiptail Lizard Cnemidophorus vanzoi (Sauria: Teiidae) microsatellite primers

Eight polymorphic microsatellite loci have been characterized for the endangered St Lucia Whiptail Lizard Cnemidophorus vanzoi. Endemic to two small islets, Maria Major and Maria Minor, off the coast of St Lucia, Lesser Antilles, the world population is estimated at < 1000 individuals. However, representatives of the systematically complex genus Cnemidophorus, containing sexual species and parthenogenetic allopolyploids, are distributed widely in North, Central and South America, and on several islands in the Caribbean Sea. These microsatellite markers are being used to monitor the genetic structure of a population of St Lucia Whiptails, recently founded through translocation, on the nearby Praslin Island.     

Resource partitioning of space and its relationship to body temperature in Anolis lizard populations

Summary An index is introduced that allows both the use and availability of space as a resource to be quantified in a manner that parallels the way that the use and availability of food resources are quantified in community ecology. This index provides the resource axis for space resources that pertains to the thermal implications of micro-climate. The index is called the Grey Body Temperature Index (GBTI) and it is the equilibrium temperature that an inanimate reference object attains in the space being quantified. For this study the inanimate reference object is a grey lizard-shaped object weighing 5 grams. Formulae to calculate the GBTI from measurements of air temperature, wind speed and solar radiation are derived from an energy balance equation. The technique is illustrated with Anolis lizard populations from Grenada and St. Kitts. It is shown that the two lizard species in Grenada partition space as a resource with respect to GBTI and that the two species in St. Kitts do not. The determination of the availability of space along the GBTI axis is illustrated for a site in St. Maarten.     

The distribution of mosquitoes across an altitudinal gradient in the Galapagos Islands

An avian malaria parasite (genus Plasmodium) has been detected consistently in the Galapagos Penguin (Spheniscus mendiculus) and less frequently in some passerines. We sampled three resident mosquito species (Aedes taeniorhynchus, Culex quinquefasciatus, and Aedes aegypti) using CDC light and gravid traps on three islands in 2012, 2013, and 2014. We sampled along altitudinal gradients to ask whether there are mosquito‐free refugia at higher elevations as there are in Hawaii. We captured both Ae. taeniorhynchus and Cx. quinquefasciatus at all sites. However, abundances differed across islands and years and declined significantly with elevation. Aedes aegypti were scarce and limited to areas of human inhabitation. These results were corroborated by two negative binomial regression models which found altitude, year, trap type, and island as categorized by human inhabitation to be significant factors influencing the distributions of both Ae. taeniorhynchus and Cx. quinquefasciatus. Annual differences at the highest altitudes in Isabela and Santa Cruz indicate the lack of a stable highland refuge if either species is found to be a major vector of a parasite, such as avian malaria in Galapagos. Further work is needed to confirm the vector potential of both species to understand the disease dynamics of avian malaria in Galapagos.     

Experimental studies of adaptive differentiation in Bahamian Anolis lizards

Populations of the lizards Anolis carolinensis and A. sagrei were experimentally introduced onto small islands in the Bahamas. Less than 15 years after introduction, we investigated whether the populations had diverged and, if so, whether differentiation was related to island vegetational characteristics or propagule size. No effect of founding population size was evident, but differentiation of A. sagrei appears to have been adaptive, a direct relationship existed between how vegetationally different an experimental island was from the source island and how much the experimental population on that island had diverged morphologically. Populations of A. carolinensis had also diverged, but were too few for quantitative comparisons. A parallel exists between the divergence of experimental populations of A. sagrei and the adaptive radiation of Anolis lizards in the Greater Antilles; in both cases, relative hindlimb length and perch diameter are strongly correlated. This differentiation could have resulted from genetic change or environmentally-driven phenotypic plasticity. Laboratory studies on A. sagrei from a population in Florida indicate that hindlimb length exhibits adaptive phenotypic plasticity. Further studies are required to determine if the observed differences among the experimental populations are the result of such plasticity. Regardless of whether the differences result from plasticity, genetic change, or both, the observation that anole populations differentiate rapidly and adaptively when exposed to novel environmental conditions has important implications for understanding the adaptive radiation of Caribbean anoles.     

Integrating phylogenetic and ecological distances reveals new insights into parasite host specificity

The range of hosts a pathogen infects (host specificity) is a key element of disease risk that may be influenced by both shared phylogenetic history and shared ecological attributes of prospective hosts. Phylospecificity indices quantify host specificity in terms of host relatedness, but can fail to capture ecological attributes that increase susceptibility. For instance, similarity in habitat niche may expose phylogenetically unrelated host species to similar pathogen assemblages. Using a recently proposed method that integrates multiple distances, we assess the relative contributions of host phylogenetic and functional distances to pathogen host specificity (functional–phylogenetic host specificity). We apply this index to a data set of avian malaria parasite (Plasmodium and Haemoproteus spp.) infections from Melanesian birds to show that multihost parasites generally use hosts that are closely related, not hosts with similar habitat niches. We also show that host community phylogenetic ß‐diversity (Pßd) predicts parasite Pßd and that individual host species carry phylogenetically clustered Haemoproteus parasite assemblages. Our findings were robust to phylogenetic uncertainty, and suggest that phylogenetic ancestry of both hosts and parasites plays important roles in driving avian malaria host specificity and community assembly. However, restricting host specificity analyses to either recent or historical timescales identified notable exceptions, including a ‘habitat specialist’ parasite that infects a diversity of unrelated host species with similar habitat niches. This work highlights that integrating ecological and phylogenetic distances provides a powerful approach to better understand drivers of pathogen host specificity and community assembly.     

Ecomorphological convergence in Eleutherodactylus frogs: a case of replicate radiations in the Caribbean

Replicate radiations, the repeated multiplication of species associated with ecological divergence, have attracted much attention and generated as much debate. Due to the few well‐studied cases, it remains unclear whether replicate radiations are an exceptional result of evolution or a relatively common example of the power of adaptation by natural selection. We examined the case of Eleutherodactylus frogs, which radiated in the Caribbean islands resulting in more than 160 species that occupy very diverse habitats. A time‐calibrated phylogeny revealed that these frogs independently diversified on all larger islands producing species that occupy a broad range of microhabitats in different islands. Using phylogenetic comparative methods, we found an association between morphological traits and particular microhabitats, and for most microhabitats detected significant morphological convergence. Our results indicate Caribbean Eleutherodactylus are a novel example of replicate radiations, and highlight the predictability of evolutionary processes, as similar ecological opportunities can lead to similar outcomes.