Heidi M. Snell

Intrapopulation variation in predator-avoidance performance of Galápagos lava lizards: The interaction of sexual and natural selection

SummaryThe interaction of sexual and natural selection in shaping variation in defensive behavior was explored via three steps. (1) Three predictions from the hypothesis that varying responses to predation account for intrapopulation variation in locomotory performance and wariness were tested. One measure of locomotory performance and two measures of wariness were compared between lava lizards (Tropidurus albemarlensis) inhabiting sparsely (1% cover) and heavily (33% cover) vegetated areas of Isla Plaza Sur in the Galapagos Archipelago. (2) Variation in morphology was examined to identify proximate mechanisms for differences seen in (1). (3) Levels of predation were compared between males and females to test a prediction from a model explaining the observed variation in defensive behavior. Male, but not female, lizards from sparsely vegetated areas were faster than those from heavily vegetated areas. Both male and female lizards from sparsely vegetated areas were significantly warier than those from heavily vegetated areas. Multiple regression, covariance, and residual analyses identify relatively longer hindlimbs of males as the proximate cause of their greater speed over that of females, rather than differences in body size, but neither body nor hindlimb size account for the microgeographic differences in speed of males. Significantly higher predation on males provided a positive test of the major prediction from our model of selective forces in which sexual selection for territory defense by males favors short approach distances (by minimizing time away from the territory caused by erroneous flight) and leads to natural selection for their increased hindlimb size and speed.

Island biogeography of Galápagos lava lizards (Tropiduridae: Microlophus): species diversity and colonization of the archipelago.

The “lava lizards” (Microlophus) are distributed throughout the Galápagos Archipelago, and consist of radiations derived from two independent colonizations. The “Eastern Radiation” includes M. bivittatus and M. habeli endemic to San Cristobal and Marchena Islands. The “Western Radiation” includes five to seven historically recognized species distributed across almost the entire Archipelago. We combine dense geographic sampling and multilocus sequence data to estimate a phylogenetic hypothesis for the Western Radiation, to delimit species boundaries in this radiation, and to estimate a time frame for colonization events. Our phylogenetic hypothesis rejects two earlier topologies for the Western Radiation and paraphyly of M. albemarlensis, while providing strong support for single colonizations on each island. The colonization history implied by our phytogeny is consistent with general expectations of an east-to-west route predicted by the putative age of island groups, and prevailing ocean currents in the Archipelago. Additionally, combined evidence suggests that M. indefatigabilis from Santa Fe should be recognized as a full species. Finally, molecular divergence estimates suggest that the two colonization events likely occurred on the oldest existing islands, and the Western Radiation represents a recent radiation that, in most cases, has produced species that are considerably younger than the islands they inhabit.

Population genetics of Galápagos land iguana (genus Conolophus) remnant populations

The Galápagos land iguanas (genus Conolophus) have faced significant anthropogenic disturbances since the 17th century, leading to severe reduction of some populations and the extinction of others. Conservation activities, including the repatriation of captive‐bred animals to depleted areas, have been ongoing since the late 1970s, but genetic information has not been extensively incorporated. Here we use nine species‐specific microsatellite loci of 703 land iguanas from the six islands where the species occur today to characterize the genetic diversity within, and the levels of genetic differentiation among, current populations as well as test previous hypotheses about accidental translocations associated with early conservation efforts. Our analyses indicate that (i) five populations of iguanas represent distinct conservation units (one of them being the recently discovered rosada form) and could warrant species status, (ii) some individuals from North Seymour previously assumed to be from the natural Baltra population appear related to both Isabela and Santa Cruz populations, and (iii) the five different management units exhibit considerably different levels of intrapopulation genetic diversity, with the Plaza Sur and Santa Fe populations particularly low. Although the initial captive breeding programmes, coupled with intensive efforts to eradicate introduced species, saved several land iguana populations from extinction, our molecular results provide objective data for improving continuing in situ species survival plans and population management for this spectacular and emblematic reptile.

Phenotypic Divergence Despite High Levels of Gene Flow in Galapagos Lava Lizards (Microlophus albemarlensis)

The extent of evolutionary divergence of phenotypes between habitats is predominantly the result of the balance of differential natural selection and gene flow. Lava lizards (Microlophus albemarlensis) on the small island of Plaza Sur in the Galápagos archipelago inhabit contrasting habitats: dense vegetation on the western end of the island thins rapidly in a transitional area, before becoming absent on the eastern half. Associated with these habitats are phenotypic differences in traits linked to predator avoidance (increased wariness, sprint speed, and endurance in lizards from the sparsely vegetated habitat). This population provides an opportunity to test the hypothesis that reduced gene flow is necessary for phenotypic differentiation. There was no evidence of any differences among habitats in allele frequencies at six out of seven microsatellite loci examined, nor was there any indication of congruence between patterns of genetic variability and the change in vegetation regime. We infer that gene flow between the habitats on Plaza Sur must be sufficiently high to overcome genetic drift within habitats but that it does not preclude phenotypic differentiation.

Temporal and Spatial Covariation of Gender and Oxidative Stress in the Galápagos Land Iguana Conolophus subcristatus

Physiological responses to organismal stress can have direct impacts on individual fitness. While responses to stressors mediated by glucocorticoid hormones are well studied, the regulation of the redox system via pro‐oxidant and antioxidant balance as well as the natural causes of oxidative stress in nature remain poorly known, especially for reptiles. In this study, we investigate the interpopulation and intersex variation in oxidative damage and plasma antioxidant capacity in the Galápagos land iguana, Conolophus subcristatus, over a 3‐yr study to evaluate what factors (e.g., season, food availability, reproductive activity) can explain levels and patterns of oxidative damage and of plasma antioxidant capacity. Our results indicate that (1) males showed lower levels of oxidative damage, higher levels of plasma antioxidant capacity, and better body condition than females and (2) significant interactions exist among patterns of oxidative damage across sexes, sampling localities, body condition, and season. These results suggest that reproductive activity and food abundance might act as determinants shaping levels and patterns of oxidative stress of land iguanas.

An overlooked pink species of land iguana in the Galápagos

Despite the attention given to them, the Galápagos have not yet finished offering evolutionary novelties. When Darwin visited the Galápagos, he observed both marine (Amblyrhynchus) and land (Conolophus) iguanas but did not encounter a rare pink black-striped land iguana (herein referred to as “rosada,” meaning “pink” in Spanish), which, surprisingly, remained unseen until 1986. Here, we show that substantial genetic isolation exists between the rosada and syntopic yellow forms and that the rosada is basal to extant taxonomically recognized Galápagos land iguanas. The rosada, whose present distribution is a conundrum, is a relict lineage whose origin dates back to a period when at least some of the present-day islands had not yet formed. So far, this species is the only evidence of ancient diversification along the Galápagos land iguana lineage and documents one of the oldest events of divergence ever recorded in the Galápagos. Conservation efforts are needed to prevent this form, identified by us as a good species, from extinction.

Progressive colonization and restricted gene flow shape island-dependent population structure in Galápagos marine iguanas (Amblyrhynchus cristatus)

BackgroundMarine iguanas (Amblyrhynchus cristatus) inhabit the coastlines of large and small islands throughout the Galápagos archipelago, providing a rich system to study the spatial and temporal factors influencing the phylogeographic distribution and population structure of a species. Here, we analyze the microevolution of marine iguanas using the complete mitochondrial control region (CR) as well as 13 microsatellite loci representing more than 1200 individuals from 13 islands.ResultsCR data show that marine iguanas occupy three general clades: one that is widely distributed across the northern archipelago, and likely spread from east to west by way of the South Equatorial current, a second that is found mostly on the older eastern and central islands, and a third that is limited to the younger northern and western islands. Generally, the CR haplotype distribution pattern supports the colonization of the archipelago from the older, eastern islands to the younger, western islands. However, there are also signatures of recurrent, historical gene flow between islands after population establishment. Bayesian cluster analysis of microsatellite genotypes indicates the existence of twenty distinct genetic clusters generally following a one-cluster-per-island pattern. However, two well-differentiated clusters were found on the easternmost island of San Cristóbal, while nine distinct and highly intermixed clusters were found on youngest, westernmost islands of Isabela and Fernandina. High mtDNA and microsatellite genetic diversity were observed for populations on Isabela and Fernandina that may be the result of a recent population expansion and founder events from multiple sources.ConclusionsWhile a past genetic study based on pure FST analysis suggested that marine iguana populations display high levels of nuclear (but not mitochondrial) gene flow due to male-biased dispersal, the results of our sex-biased dispersal tests and the finding of strong genetic differentiation between islands do not support this view. Therefore, our study is a nice example of how recently developed analytical tools such as Bayesian clustering analysis and DNA sequence-based demographic analyses can overcome potential biases introduced by simply relying on FST estimates from markers with different inheritance patterns.

A survey of the coccidian parasites of reptiles from islands of the Galápagos Archipelago: 1990-1994.

From 1990 through 1994, fecal samples were collected and examined for coccidian parasites from 26 giant land tortoises Geochelone nigra, from 715 lava lizards Tropidurus spp., from 139 land iguanas Conolophus subcristatus, and from 128 marine iguanas Amblyrhynchus cristatus, all of which inhabit various islands in the Galápagos Archipelago. None of the samples from A. cristatus or from C. subcristatus was infected with coccidia. Only 1 of 26 (4%) G. nigra was infected with a single Eimeria species that we describe here as new. A total of 262 of 715 (37%) individuals representing 3 species of Tropidurus discharged oocysts of 1-3 different coccidian species; these included 2 previously described species Eimeria tropidura and Isospora insularius, and an eimerian that we describe here as new. Additionally, 104 fecal samples from Tropidurus spp. were from 51 animals recaptured in either 2 or 3 yr; 21 had no infections in any year, 15 were infected at least once, 14 were infected in 2 yr, and only 1 was infected during 3 yr. No animal was recaptured and sampled during each of the 4 yr of this study. Of the 262 infected individuals, 30 (12%) had multiple coccidial infections at the time of collection (eimerian and isosporan, or 2 eimerians). Where determination of the sexes was possible in the lava lizards, there was no difference in prevalence rates between males (39%) and females (41%). Sporulated oocysts of the new eimerian from Tropidurus are ellipsoidal, 27.1 x 15.6 (25-31 x 14-18) microns, with a polar body, but without a micropyle or oocyst residuum; they contain ellipsoidal sporocysts, 11.8 x 6.7 (10-14 x 6-8) microns, without Stieda, sub-, or parastieda bodies, but with a sporocyst residuum. Sporulated oocysts of the new eimerian from G. nigra are ellipsoidal to ovoidal, 21.6 x 18.1 (18-25 x 16-20) microns, with a large polar body, but without a micropyle or oocyst residuum; they contain ellipsoidal sporocysts 10.7 x 7.0 (8-12 x 5-8) microns, with Stieda body but no sub- or parastieda bodies. Also present is a sporocyst residuum of medium to large granules randomly distributed among the sporocysts.

Ancient DNA gives green light to Galápagos Land Iguana repatriation

Land Iguanas, Conolophus subcristatus,were extirpated from Isla Baltra, GalápagosArchipelago in the 1940s. Historical recordsindicate that some Baltra iguanas weretranslocated to nearby Isla Seymour Norte inthe 1930s. Plans to repatriate iguanas toBaltra were suspended when evidence suggestedthat iguanas on Seymour Norte may not beentirely of Baltra origin. Comparison of DNAfrom century-old museum specimens with extantiguanas has identified those individuals ofunambiguous Baltra origin on Seymour Norte. These results provide scientific criteria forthe ecological restoration of these endangeredreptiles.

The variation and genetic basis of dorsal color pattern in the desert side-blotched lizard, Uta stansburiana stejnegeri

We investigated quantitative variations and inheritance of the dorsal color pattern of Uta stansburiana stejnegeri exclusive of the strongly sexually dichromatic spotting pattern. The color pattern was quantified by measuring both the variation in stripe width and the proportion of the body that was striped. Each measurement technique resulted in a single value representing the color pattern of each individual. There was no strong quantitative relationship between variations of the color pattern either of mothers and sons or mothers and daughters. Therefore, heritability, if present, could not be detected. However, the color patterns of mothers and daughters tended to be similar, but the color patterns of mothers and sons differed significantly