The microevolution of the Galápagos marine iguana Amblyrhynchus cristatus assessed by nuclear and mitochondrial genetic analyses

Marine iguanas may have inhabited the Galápagos archipelago and its former, now sunken islands for more than 10 million years (Myr). It is therefore surprising that morphological and immunological data indicate little evolutionary divergence within the genus. We utilized mitochondrial DNA (mtDNA) sequence analyses and nuclear DNA fingerprinting to re-evaluate the level and pattern of genetic differentiation among 22 marine iguana populations from throughout the archipelago. Both genetic marker systems detect a low level of within-genus divergence, but they show contrasting levels of geographical subdivision among the populations. The mitochondrial gene pools of populations from different regions of the archipelago are isolated, and the mtDNA pattern appears to follow the sequence in which the islands were colonized by marine iguanas. Conversely, the nuclear DNA study indicates substantial interpopulational gene exchange, and the geographical distribution of the nuclear markers seems to be determined by isolation by distance among the populations. The natural history of marine iguanas suggests that the contrasting nuclear and mitochondrial DNA patterns result from an asymmetric migration behaviour of the two sexes, with higher (active and passive) interisland dispersal for males than females. Separate genetic analyses for the sexes appear to support this hypophesis. Based on these findings, a scenario is proposed that explains the marine iguanas' low genetic divergence, notwithstanding their long evolutionary history in the Galápagos archipelago.     

A set of highly discriminating microsatellite loci for the Galápagos marine iguana Amblyrhynchus cristatus

We describe here the cloning of 12 (7 dinucleotide, 1 trinucleotide and 4 tetranucleotide) microsatellite loci for the Galápagos marine iguana Amblyrhynchus cristatus. When tested for individuals from five different island populations on the Galápagos archipelago, high genetic diversities (9–20 alleles per locus) and heterozygosities (0.200–0.944) were observed. All loci showed no obvious deviations from Hardy–Weinberg equilibrium. The new set of microsatellite loci was able to assign individuals reliably to their island of origin, thus being able to discriminate between residents and migrants between islands.     

Ontogenetic changes in food intake and digestion rate of the herbivorous marine iguana (Amblyrhynchus cristatus,Bell)

Young reptiles have higher relative energy demands than adults, but the proposed ontogenetic changes in diet to fulfil these demands were not found in the algae-eating Galápagos marine iguanas on Santa Fé. Feeding and digestion rates were investigated to analyse how young achieve higher energy intake. Daily food intake of free ranging marine iguana hatchlings (6–11 months old) was about one third that of adults, but relative intake (g dry mass · g^–1 wet mass · day^–1) was four times higher in the hatchlings. During feeding experiments, relative daily food intake of hatchling marine iguanas was approximately three times higher than that of adults (0.042 vs 0.013 g dry mass · g^–0.8 wet mass · day^–1), and mean gut passage time was two times shorter (5 vs 10 days). The hatchlings also maintained high body temperatures (36.7° C) even under relatively cool day-time air temperatures of 32° C. Apparent digestibility of algal food measured both during feeding trials and by Mn²⁺ AAS (atomic absorption spectrometry) for free-ranging iguanas was 70%, independent of body size and temperature. The red algae prevailing in the diet were high in protein (30% dry mass) and energy (12.1 kJ/g dry mass). Diving iguanas had higher rates of energy intake than intertidal foragers, but daily intake was less. Maintenance of high body temperature enabled hatchlings to achieve high digestion rates and, combined with high relative intake, thus achieve sufficient energy intake for rapid growth despite higher mass specific metabolic rates. Estimates of biomass of marine iguanas and their algal food are given for a section of coastline on Santa Fé.     

Recent research on the evolution of land birds on the Galápagos

A decade of research on the evolution of Galápagos land birds is reviewed, and outstanding questions to be answered are highlighted. Evolutionary studies have been restric 1 almost entirely to the four species of mockingbirds and the 13 species of Darwin's finches. Long-term field studies have been initiated on representatives of both groups. Co-operative breeding has been discovered in the mockingbirds (and hawks).
Lack's (1945, 1947) monographic treatment of Darwin's finches has been largely upheld and extended by morphological, ecological, behavioural and biochemical studies. While the phylogenetic origins of Darwin's finches still remain uncertain, the major groupings of the finches have been confirmed by the results of protein polymorphism analysis. Fossils of Darwin's finches have been discovered recently: their potential for illuminating evolutionary change has not yet been realized. Three other major developments are (1) quantitative confirmation of the role of interspecific competition in the adaptive radiation, (2) experimental confirmation of the role of morphological and song cues in species recognition, and experimental evidence of their evolution in the speciation process, and (3) direct study of natural selection on heritable quantitative traits in a population, and identification of its causes. Continuing studies of population variation are likely to reveal the contemporary importance of selection, migration and hybridization, and thereby help us to more fully understand the causes of the adaptive radiation of Darwin's finches.     

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.     

Taxonomy and phytogeny of the genus Acalypha (Euphorbiaceae) in the Galápagos Archipelago

A preliminary phylogeny of the Neotropical Acalypha is proposed, and previous infrageneric classifications commented upon. New views are presented on the floral morphology; the homology of the inflorescences and of the allomorphic female flower. The Galapagos Acalypha (Euphorbiaceae, Acalyphinae) are revised; the group is established as monophyletic and its relationships are shown. The sister–group is the Neotropical A. cuspidata–complex. Four species are recognized, viz. A. baurii Robinson & Greenman, A. wiggensii Webster, A. parvula J. D. Hooker, and A. abingdonii sp. nov. A. baurii is shown to be the sister–group of A. abingdonii + A. wigginsii+A. parvula, and A. abingdonii the sister–group of A. wigginsii + A. parvula. Brief accounts are given on nomenclatural history, aspects of morphology, chromosome numbers, geographical distribution (incl. the biogeography of the Galapagos Isles), ecology, pollination biology, and population structure. Se propone una filogenia preliminar para la Acalypha neotropical y se comenta la clasificacion infragenerica anterior. Se presenta nuevos puntos de vista sobre la morfología floral, la homología de las infloresciencias y sobre las floras alomórficas femeninas. Se revisa nomenclatura y taxonomía de Acalypha de Galápagos (Euphorbiaceae, Acalyphinae); se establece el grupo como monofilético y se revelan sus relaciones: el grupo gemelo es el complejo A. cuspidata neotropical. Se reconoce cuatro especies en esta revision: A. baurii Robinson & Greenmann, A. wigginsii Webster, A. parvula J. D. Hooker, y una nueva, A. abingdonii que se describe. A. baurii parece ser gemela de A. abingdonii + A. wigginsii + A. parvula, y A. abingdonii la gemela de A. wigginsii + A. parvula. Se hace comentarios cortos sobre la historia de la nomenclatura, aspectos de morfologia, numero cromosonico, dis–tribusión geografica (incluyendo la biogeografía de las Islas Galápagos), ecologia, biología de polinizaci6n y estructura poblacional.     

Scalesia gordilloi sp. nov. (Asteraceae) from the Galápagos Islands, Ecuador

Scalesia gordilloi está descrita desde la isla San Cristóbal, Islas Galápagos, Ecuador. Tiene una distribución limitada y local al lado de la costa sur en la zona vegetal árida. Está relacionada a S. divisa Anderss. y S. incisa Hook. f. Se discute la taxonomía de S. gordilloi.     

A new look at evolution in the Galápagos: evidence from the late Cenozoic marine molluscan fauna

Endemism is not as common in the marine invertebrate fauna of the Galápagos Islands region as in the adjacent terrestrial biota. Marine invertebrates in the Galápagos are largely cosmopolitan species from the Panamic, Indo-Pacific, Californian, or Peruvian faunal provinces. However, an endemic component is also present in the fauna. The observed pattern among marine invertebrate organisms can be accounted for by at least two processes: (1) genetic continuity between mainland and island populations mediated through planktonic larvae; and (2) lower rates of intrinsic evolutionary change. The evolutionary scenario standardly applied to terrestrial organisms in the Galápagos, namely, adaptive radiation and speciation in reproductive isolation from mainland source populations, does not apply to all marine invertebrates. Evidence in support of the alternative scenario for marine invertebrates comes from both published records of species occurring in the islands and recent studies of fossil-bearing deposits on several islands in the archipelago. Two misconceptions–considering the islands and sedimentary deposits to be older than now thought, and equating the rate of evolution of the terrestrial biota with the marine biota–can lead to an incorrect interpretation of evolution in the Galápagos Contrasts between marine invertebrate and terrestrial organisms serve to illustrate some fundamental differences which have important evolutionary implications. Some of these are: endemism; dispersal; taxonomic relationships; island definitions; rates of evolutionary change; and age of fossils. In terms of Darwin's evolutionary scenario, terrestrial organisms represent the paradigm and marine organisms represent the paradox.     

Age-related changes in hematocrit in the Galápagos sea lion (Zalophus wollebaeki) and the Weddell seal (Leptonychotes weddellii)

In mammals, hematocrit (Hct) is optimized between the divergent requirements of blood flow characteristics and oxygen transport and storage capacity. This trade‐off plays a particularly major role in marine mammals, in which oxygen demand during sustained diving requires high Hct levels. Galápagos sea lions (Zalophus wollebaeki) need a long time after birth to develop from terrestrial life to the state of an independent forager at sea. We here show that pups were born with high Hct of 45%, then reduced Hct during the first 40 d of life to 31% while they remain constantly ashore, and increased Hct again until the adult level (57%) is reached at 1 yr of age when they begin to dive for foraging at sea. A similar, but much more rapidly changing pattern is seen in Weddell seal pups, but not in northern elephant seals, where no reduction in Hct is seen after birth. These and similarly changing patterns in terrestrial mammals likely reflect species specific functional adjustments during development due to a trade‐off between the costs of circulation and the changing need to store and transport oxygen.     

Flightlessness in the Galápagos cormorant (Compsohalieus [Nannopterum] harrisi): heterochrony, giantism and specialization

A study of flightlessness in the Galápagos cormorant (Compsohalieus [Nannopterum] harrisi) was undertaken using study skins and skeletons of C. harrisi and eight flighted confamilials; in addition, four skin specimens and disassociated skeletal elements of the extinct spectacled cormorant (C. perspicillatus) of Beringia, reputed by some to have been flightless, were studied. Anatomical specimens of C. penicillatus and C. harrisi were dissected for myological comparisons. Flightless C. harrisi is 1.6 to 2.2 times as heavy as its extant flighted congeners; males averaged 3958 g and females averaged 2715 g in total body weight. Estimates of body weight for C. perspicillatus based on femur length approximated 3900 g. Wing lengths of C. harrisi were smaller than those of any other cormorant, averaging 190 mm and 170 mm for males and females, respectively. Wing-loadings (g body mass.cm^-2 wing area) of flighted cormorants ranged from 1.0 to 1.7. Estimated wing-loadings, incorporating approximate wing areas, were 2.0 and 5.1 g.cm^-2 for C. perspicillatus and C. harrisi, respectively; the former suggests that C. perspicillatus was probably capable of laboured flight. The small wings of C. harrisi result from an c. 50% shortening of remiges, accompanied by reduced asymmetry of vane widths and increased rounding of the tips, and significant reductions in lengths of wing bones, particularly the radius and ulna. Numbers of primary and secondary remiges in C. harrisi remain unchanged. Multivariate morphometries revealed that sexual dimorphism in external and skeletal dimensions is significantly greater in C. harrisi than in flighted cormorants. Canonical analysis of six external measurements indicated that C. harrisi is distinguished primarily by its relatively short wings. Skeletal peculiarities of C. harrisi were diverse, including conformational changes in the sternum, furcula, coracoid, humerus, ulna, radius, carpometacarpus and patella. Mensural comparisons confirmed substantial reductions in elements of the pectoral girdle of C. harrisi, particularly the sternal carina, as well as the alar skeleton, especially the radius and ulna. Differential shortening of the wing elements resulted in significant differences in proportions within the wing skeleton. These unique skeletal proportions of C. harrisi, in addition to its great overall size, combine to produce an immense multivariate skeletal distance between C. harrisi and all confamilials. Sexual dimorphism in skeletal dimensions, in both total and size-corrected data, was 2–3 times greater in C. harrisi than in other phalacrocoracids sampled. Most pectoral muscles of C. harrisi were absolutely or relatively smaller than those of C. penicillatus, in spite of its larger body size. No muscles or parts thereof were lacking in the pectoral limb of C. harrisi, but a number of qualitative differences distinguished the musculature of the flightless species, including: an exceptionally tough skin involving a well-developed M. pectoralis pars abdominalis and M. latissimus dorsi interscapularis; a thin, medially obsolete and laterally extensive M. pectoralis pars thoracica; a weakly developed M. rhomboideus profundus consisting of a variably tendinous fascia invested with three fasciculi of muscle fibres; an extraordinarily thick, extensive M. obliquus externus abdominis, which, together with a unique cnemio-costal slip of smooth muscle, restricts the metapatagium through an anchoring of M. serratus superficialis metapatagialis; and the presence of a unique alular muscle named here as M. levator alulae. Fusions of the tendons of origin and insertion, respectively, of M. flexor digiti superficialis and M. flexor digiti profundus in C. harrisi, muscles derived from a common muscle primordium, and the retention of a carpometacarpal tendon of M. flexor carpi ulnaris cranialis constitute strong evidence of pectoral paedomorphosis in C. harrisi. Mensural comparisons quantified the reduction of pectoral muscles in C. harrisi and indicated that these reductions were especially pronounced in the distal musculature. Morphological characteristics of Phalacrocoracidae, together with the exploitation of localized marine food resources and weakly developed seasonal movements of Compsohalieus, may have predisposed the founding population of C. harrisi to flightlessness. Anatomical changes in C. harrisi are exceeded in degree among foot-propelled diving birds by those of only a few fossil flightless birds (e.g. Hesperomis, Chendytes). Many of the morphological peculiarities of C. harrisi are paedomorphic, although several are not attributable to developmental heterochrony. These morphological characters of flightless C. harrisi are considered with respect to locomotion, feeding ecology, reproduction and demography of the species, and are compared with those of other flightless carinates.     

The classical case of character release: Darwin's finches (Geospiza) on Isla Daphne Major, Galápagos

The history of how Darwin's medium ground finch (Geospiza fortis) on Isla Daphne Major, Galápagos became a textbook example of character release is reviewed. Four hypotheses for the evolution of the intermediate-sized Daphne fortis are examined, including genetic drift/founder effect, hybridization with the small ground finch (G'. fuliginosa) , food supply (or local adaptation hypothesis) and character release in allopatry.
Modern data suggest that genetic drift is unlikely to have been important, due to inadequate isolation and over-riding selection and introgression on Daphne. All three remaining hypotheses have probably played a role. Hybridization with G. fuliginosa occurs, although it cannot counteract the selection pressures seen during our study. Local adaptation has also occurred, with natural selection changing the relative frequencies of fortis phenotypes in response to changes in Daphne food supplies. The selection resulted from correlations between the size of seeds available, feeding behaviour and morphology. However, recent phenotypic tracking has resulted in larger, not smaller phenotypes. There is also evidence for character release in the form of diet expansion by G. fortis during periods of food shortage, and indirect evidence for interspecific competition between fortis and the cactus ground finch (G. scandens). The Daphne fortis phenotype probably represents a balance between introgression with fuliginosa, selection for larger body size in dry years and selection for smaller body size in wet years. The simple textbook account of a character shift caused by the accidental absence of competitors should be qualified to reflect the ecological complexity of the situation.     

Genetic differentiation and speciation in Stomion (Goleoptera: Tenebrionidae): flightless beetles of the Galápagos Islands, Ecuador

Stomion is a swarm of 13 tenebrionid beetle taxa endemic to the Galápagos Islands. The taxa show marked morphological variation, and all are flighdess. They can be divided into three divergent morphological groups based on external sculpturing of the elytra. Eleven taxa were examined electrophoretically at 20 enzyme loci to measure the extent of genetic differentiation which accompanied morphological differentiation and speciation. Stomion are shown to be ideal candidates for allopatric and founder event speciation, with their limited dispersal ability, narrow distributions, and incidence of single-island endemics. Accordingly, individual heterozygosities were low in most taxa, and gene pool divergence was apparent among populations of single taxa occupying different islands. Both interspecific and intraspecific genetic identities were high, with an average 1 = 0.88 and I = 0.96, respectively. The relatively young age of the genus and the allopatric mode of speciation may account for high genetic relatedness. No clear relationship was found between allozyme phenotypes and the three morphological groups, thus, the evolution of these traits may have been facilitated by similar selection among islands of similar age and geography. The geographical distributions of the morphological groups can be used to suggest a general pattern of speciation for the group.     

Structure of a plant-pollinator network on a pahoehoe lava desert of the Galápagos Islands

Plant-pollinator interactions are important for the evolution and survival of the species involved. Plant-pollinator networks on oceanic islands are often small in size and as a consequence the connectance is high suggesting a substantial generalisation level. Further, linkage level for insular plants is shown to be lower than on mainland. The present study investigates a plant-pollinator network on the Galápagos Islands that is unique because of its very small size. We recorded pollinator visits to plant species as well as pollen grains on insect bodies. The combination of these data increased the observed number of interactions. The values for connectance and linkage level for plants were found to be consistent with similar values found in other network studies. There were no relation between the abundance of plant species and the number of pollinating species. The dominating pollinator species was the Galápagos carpenter bee Xylocopa darwini . Specimens of the shorthorned grasshopper Halmenus cuspidatus turned out to carry pollen from five plant species out of twelve and are probably functioning as pollinator. Bagging experiments revealed dependency on insect visits for a high seed set for most of the plant species, but only one species Plumbago scandens seemed to possess a pollen limited seed set. The network showed an asymmetric pattern of number of interactions per species with a few species having several interactions and many species a few. This pattern is supposed to result in a rather robust community, but is also fairly sensitive if the dominant species are threatened. The high connectance value found could, however, counteract this vulnerability.     

Effects of foraging mode and season on the energetics of the Marine Iguana, Amblyrhynchus cristatus

1. Marine Iguanas ( Amblyrhynchus cristatus ) inhabiting the rocky shores of the Galápagos Islands apply two foraging strategies, intertidal and subtidal foraging, in a seasonal climate. Effects of both foraging strategy and seasonality on the daily energy expenditure (DEE) were measured using doubly labelled water.
2. Difference in foraging mode did not result in significant differences in DEE.
3. On Santa Fé the DEE in the warm season was significantly higher than in the cool season (67·8 ± 21·8 kJ kg^–0·8 day^–1 vs 38·0 kJ kg^–0·8 day^–1). This difference can be explained by body temperature. A model estimate of the body temperature was used to predict monthly DEE figures, giving a year round budget. On average a 1-kg iguana would need only 47 kJ day^–1, or 17 mJ year ^–1. This is lower than previous estimates in which body temperatures were not taken into account.
4. The water flux of the Marine Iguana increases with increasing foraging time. The linear rise per minute foraging is roughly two times as high for subtidally foraging animals as for intertidal foragers.     

Seasonal Changes of Vocal Rates and Their Relation to Territorial Status in Male Galápagos Sea Lions (Zalophus wollebaeki)

Male vocal displays play an important role in sexual selection through both male–male competition and female choice. While this is supported by numerous studies in birds, much less attention has been paid to the role of such displays in mammals. We investigated the function of vocal displays in a polygynous mammal, the Galápagos sea lion (Zalophus wollebaeki). In our study population a large proportion of mature males are unable to establish a territory, providing the opportunity to compare the vocal behaviour between territorial and non‐territorial males. We examined how seasonal patterns of vocalizations differed between territorial and non‐territorial males and how the number of females present in a territory influenced behaviour of territorial males. We found that territorial males vocalized at higher rates than non‐territorial males, and territorial males vocalized more at the onset than towards the end of territory tenure. During the onset of territory‐tenure vocalizations of territorial males were directed more often towards other males than females. Furthermore, we found that vocalizations of territorial males were not only given in male–male interactions, but were also actively directed towards females. Territorial males vocalized at higher rates when more females were present in their territory. Our results suggest that vocalizations are important in male–male interactions, are relevant in territorial disputes and are used as a proxy for females to assess a male’s quality.     

Number of endemic and native plant species in the Galápagos Archipelago in relation to geographical parameters

By simple and multiple regression analyses we investigate updated species numbers of endemic and native vascular plants and seed plants in the Galápagos Archipelago in relation to geographical parameters. We find that the best models to describe species numbers are regression models with log-transformed species numbers as dependent and log-transformed modified area (i.e. area not covered with barren lava) as an independent variable. This holds both for total species number, for native species number, for endemic species number and for total number of seed plants as well as number of endemic seed plants. For the ratio between endemic and native species, modified area is also the major significant variable, but with a negative regression slope.
Multiple regression models show that some isolation measures are significant contributors and may explain some of the residual variation, but their contribution to total explained variation is in general small.
The results show that the species area relationships are different for native and endemic species. This is discussed in relation to classical island biogeographical models, and the concepts of radiative speciation.     

Hybridization between Taeniatherum caput-medusae and Triticum aestívum (Poaceae)

Hybrid plants were obtained in an intergeneric cross between Taenìatherum caputmedusae (2n = 2x = 14) and Triticum aestívum (2n = 6x = 42). The chromosome number was as expected 2n = 28. Morphologically the offspring looked like Triticum aestívum . Analysis of meiotic metaphase I showed an unexpected high number of bi- and trivalents which is ascribed to homoeologous pairing of chromosomes from T. aestivum . It is concluded that the genome of Taeniatherum has effects on the pairing regulation system present in T. aestívum .