Molecular phylogeny of Mentawai macaques: taxonomic and biogeographic implications

In order to elucidate the evolutionary history and taxonomy of the Mentawai macaques, we sequenced a 567 base pairs (bp) long fragment of the mitochondrial cytochrome b gene from 39 individuals representing pigtailed macaque populations from Siberut, Sipora, South Pagai, and Sumatra. Pairwise difference analyses carried out within and among populations have shown, that: (1) variation within populations is relative low, (2) variation among populations is increased, and (3) pairwise differences within and among the populations from Sipora and South Pagai are in the same range. From phylogenetic tree reconstructions including further macaque species, we detected a paraphyletic origin of Mentawai macaques with the Siberut population more closely related to Macaca nemestrina from Sumatra, than it is to populations from the Southern islands. Based on these results, we favour a scenario in that macaques entered the Mentawai islands by two independent colonisation events. Taking together the paraphyletic origin of Mentawai macaques and the genetic differences detected among pigtailed macaque populations, which are comparable with those observed among the seven Sulawesi macaque species, we propose to separate macaques from Siberut and Sipora, North and South Pagai into two distinct species, Macaca siberu and Macaca pagensis, respectively.     

High variability of genetic pattern in giant clam (Tridacna maxima) populations within French Polynesia

Nine populations of giant clams, Tridacna maxima, from six islands of French Polynesia were screened for allozyme variation at ten polymorphic loci. The genetic structure of populations of T. maxima were studied at different spatial scales: within an island, between islands of the same archipelago and between archipelagos. Significant genetic differences were observed only between populations from different archipelagos, and genetic differentiation was correlated with geographical separation. However, these results were only supported by a single locus, PEP * and all other loci were homogeneous between studied populations. According to Lewontin & Krakauer's model, the genetic structure can be explained by selection. The selective factors most likely depend on the respective habitat of each archipelago. We also studied genotype–phenotype correlation using the colour of the clam mantle, and did not find any relationship between the mantle colour and the genetic structure of the individuals.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 221–231.     

Isolation and biodiversity in Cytisus villosus Pourret (Fabaceae,Genisteae): enzyme polymorphism in disjunct populations

ABSTRACT

The genetic diversity of isolated populations of Cytisus villosus has been studied by means of enzyme polymorphism analysis. Two types of isolated populations were studied: “terrestrial islands” in Sicily, and “true islands” in the Aeolian archipelago. In the populations of “true islands” the number of alleles and the heterozygosity are lower than in “terrestrial islands”. Isolation amongst Sicilian populations seems to be more recent than isolation of the Aeolian populations, and may be attributed to climatic changes which occurred during the Holocene and/or to human activities. The disjunction of the Aeolian populations seems much more recent than the origin of the isles themselves; the colonization of the archipelago is attributed to a single, recent dispersal event not followed by local evolution. In view of the biological structure of the Aeolian populations, C. villosus must be regarded as a locally endangered species.     

Genetic structure of house mouse (Mus musculus Linnaeus 1758) populations in the Atlantic archipelago of the Azores: colonization and dispersal

We analyzed the genetic structure and relationships of house mouse (Mus musculus) populations in the remote Atlantic archipelago of the Azores using nuclear sequences and microsatellites. We typed Btk and Zfy2 to confirm that the subspecies Mus musculus domesticus was the predominant genome in the archipelago. Nineteen microsatellite loci (one per autosome) were typed in a total of 380 individuals from all nine Azorean islands, the neighbouring Madeiran archipelago (Madeira and Porto Santo islands), and mainland Portugal. Levels of heterozygosity were high on the islands, arguing against population bottlenecking. The Azorean house mouse populations were differentiated from the Portuguese and Madeiran populations and no evidence of recent migration between the three was obtained. Within the Azores, the Eastern, Western, and Central island groups tended to act as separate genetic units for house mice, with some exceptions. In particular, there was evidence of recent migration events among islands of the Central island group, whose populations were relatively undifferentiated. Santa Maria had genetically distinctive mice, which may relate to its colonization history. © 2013 The Linnean Society of London     

Diversity despite dispersal: colonization history and phylogeography of Hawaiian crab spiders inferred from multilocus genetic data

The Hawaiian archipelago is often cited as the premier setting to study biological diversification, yet the evolution and phylogeography of much of its biota remain poorly understood. We investigated crab spiders (Thomisidae, Mecaphesa ) that demonstrate contradictory tendencies: (i) dramatic ecological diversity within the Hawaiian Islands, and (ii) accompanying widespread distribution of many species across the archipelago. We used mitochondrial and nuclear genetic data sampled across six islands to generate phylogenetic hypotheses for Mecaphesa species and populations, and included penalized likelihood molecular clock analyses to estimate arrival times on the different islands. We found that 17 of 18 Hawaiian Mecaphesa species were monophyletic and most closely related to thomisids from the Marquesas and Society Islands. Our results indicate that the Hawaiian species evolved from either one or two colonization events to the archipelago. Estimated divergence dates suggested that thomisids may have colonized the Hawaiian Islands as early as ~10 million years ago, but biogeographic analyses implied that the initial diversification of this group was restricted to the younger island of Oahu, followed by back-colonizations to older islands. Within the Hawaiian radiation, our data revealed several well-supported genetically distinct terminal clades corresponding to species previously delimited by morphological taxonomy. Many of these species are codistributed across multiple Hawaiian Islands and some exhibit genetic structure consistent with stepwise colonization of islands following their formation. These results indicate that dispersal has been sufficiently limited to allow extensive ecological diversification, yet frequent enough that interisland migration is more common than speciation.     

Molecular phylogeny of the endemic Philippine rodent Apomys (Muridae) and the dynamics of diversification in an oceanic archipelago

We analysed the phylogenetic relationships of ten of the 13 known species of the genus Apomys using DNA sequences from cytochrome b . Apomys, endemic to oceanic portions of the Philippine archipelago, diversified during the Pliocene as these oceanic islands arose de novo . Several of the speciation events probably took place on Luzon or Mindanao, the two largest, oldest, and most topographically complex islands. Only one speciation event is associated with vicariance due to Pleistocene sea-level fluctuation, and a Pleistocene diversification model in which isolation is driven by sea-level changes is inconsistent with the data. Tectonic vicariance is nearly absent from the Philippines, in which tectonic coalescence plays a significant role. Most speciation events (about two-thirds) are associated with dispersal to newly developed oceanic islands. The data imply that the species have persisted for long periods, measured in millions of years after their origins; further implications therefore are that faunal turnover is very slow, and persistence over geological time spans is more prominent than repeated colonization and extinction. Neither the equilibrium nor the vicariance model of biogeography adequately encompasses these results; a model incorporating colonization, extinction, and speciation is necessary and must incorporate long-term persistence to accommodate our observations.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society, 2003, 80 , 699–715.     

Origin of the Sulawesi macaques (Cercopithecidae: Macaco) as suggested by mitochondrial DNA phylogeny

One of the sharpest biogeographical transitions in the world occurs between the Indonesian islands of Borneo and Sulawesi; this transition is demarcated by Wallace's line. Macaque monkeys represent an interesting anomaly to faunal distributions in this region as they occur on both sides of Wallace's line, with Macacafascicularis, M. nemestrina and other species to the west and seven Sulawesi species to the east. We have investigated macaque evolution and dispersal in the Sunda region and Sulawesi using phylogenetic analysis of mitochondrial DNA sequences. Female philopatry of macaques, which causes sharp geographic clustering of maternally inherited mitochondrial DNA haplotypes, makes mitochondrial phytogenies particularly useful for investigating ancient patterns of dispersal. Results of this study suggest the following: (1) M. fascicularis is not a sister taxon to any species of Sulawesi macaque; (2) haplotypes of some M. nemestrina have a sister relationship to northern and central Sulawesi macaques, while haplotypes of other M. nemestrina have a sister relationship to soudiern Sulawesi macaques; (3) Sulawesi was probably colonized by macaques twice, once to the base of the northern peninsula now occupied by M. hecki and once to the southwestern peninsula now occupied by M, mama; and (4) within north/central and southern Sulawesi, patterns of dispersal are largely consistent with contemporary and past geography of the island, with the exception of a geographically discontinuous relationship between M. nigra and a portion of M. tonkeana from a region in northwest central Sulawesi.     

Implications of contrasting patterns of genetic variability in two vespertilionid bats from the Indonesian archipelago

Wallacean island populations of two Vespertilioninae bats, Myotis muricola and Scotophilus kuhlii , which have similar geographical ranges, showed marked contrast in the amount and pattern of genetic variation. Within islands, genetic variation was on average much higher in M. muricola but declined from west to east, whereas all populations of S. kuhlii had uniformly low levels of genetic variation by mammalian standards. S. kuhlii showed little genetic differentiation between islands and estimates of gene flow were substantial whereas island populations of M. muricola differed markedly and there was a strong isolation-by-distance effect associated with the extent of the sea crossing between islands. Furthermore, the lower mean heterozygosity and small genetic distances between eastern island populations of M. muricola is evidence that there has been a bottleneck associated with the colonization of this area. The attenuation of genetic diversity to the east is also seen in some other mammalian species and may indicate limits to dispersal and have implications for species management. The patterns of variability in S. kuhlii may be a consequence of its strong dispersal capacity and close association with human activity, which, together with other factors, suggest a panmictic population.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 421–431.     

Behavioral measurement of temperament in male nursery‐raised infant macaques and baboons

We define temperament as an individual's set of characteristic behavioral responses to novel or challenging stimuli. This study adapted a temperament scale used with rhesus macaques by Schneider and colleagues [American Journal of Primatology 25:137–155, 1991] for use with male pigtailed macaque (Macaca nemestrina, n = 7), longtailed macaque (M. Fascicularis, n = 3), and baboon infants (Papio cynocephalus anubis, n = 4). Subjects were evaluated twice weekly for the first 5 months of age during routine removal from their cages for weighing. Behavioral measures were based on the subject's interactions with a familiar human caretaker and included predominant state before capture, response to capture, contact latency, resistance to tester's hold, degree of clinging, attention to environment, defecation/urination, consolability, facial expression, vocalizations, and irritability. Species differences indicated that baboons were more active than macaques in establishing or terminating contact with the tester. Temperament scores decreased over time for the variables Response to Capture and Contact Latency, indicating that as they grew older, subjects became less reactive and more bold in their interactions with the tester. Temperament scores changed slowly with age, with greater change occurring at younger ages. The retention of variability in reactivity between and within species may be advantageous for primates, reflecting the flexibility necessary to survive in a changing environment. Am. J. Primatol. 47:43–50, 1999. © 1999 Wiley‐Liss, Inc.     

How old is the Hawaiian biota? Geology and phylogeny suggest recent divergence.

This study quantifies long-term landscape changes in the Hawaiian archipelago relating to dispersal, speciation and extinction. Accounting for volcano growth, subsidence and erosion, we modelled the elevations of islands at time intervals of 0.5 Myr for the last 32 Myr; we also assessed the variation in the spacing of volcanoes during this period. The size, spacing and total number of volcanic islands have varied greatly over time, with the current landscape of large, closely spaced islands preceded by a period with smaller, more distantly spaced islands. Considering associated changes in rates of dispersal and speciation, much of the present species pool is probably the result of recent colonization from outside the archipelago and divergence within contemporary islands, with limited dispersal from older islands. This view is in accordance with abundant phylogenetic studies of Hawaiian organisms that estimate the timing of colonization and divergence within the archipelago. Twelve out of 15 multi-species lineages have diverged within the lifetime of the current high islands (last 5 Myr). Three of these, and an additional seven (mostly single-species) lineages, have colonized the archipelago within this period. The timing of colonization of other lineages remains uncertain.     

Wallace’s line revisited: has vicariance or dispersal shaped the distribution of Malesian hawkmoths (Lepidoptera: Sphingidae)?

Large-scale biogeographical patterns of Sphingidae in the Malesian archipelago are investigated, using Geographic Information System-supported estimates of species ranges determined from a compilation of specimen-label databases. Distribution maps for all species and checklists for 114 islands are presented at http://www.sphingidae-sea.biozentrum.uni-wuerzburg.de . Phenetic analyses of island faunas reveal 'textbook'-like patterns of biogeographical associations in the region, with Wallace's line emerging as the main faunal discontinuity in the region. Further analyses, using partial Mantel statistics, indicate that historical features of geography (such as land bridges formed during periods of lower sea levels) are an important determinant of faunal similarity, but recent dispersal can also explain a significant portion of present day hawkmoth distributions. Faunal turnover in relation to distance between islands is steeper for Smerinthinae than for other subfamilies, indicating different dispersal abilities among higher taxonomic groups. These differences are discussed in the light of life-history differences between the subfamilies. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 455–468.     

A case of pulmonary cestodiasis in a simian immunodeficiency virus-infected pigtailed macaque (Macaca nemestrina) in which virus-infected leukocytes are present within the lesion

Abstract: The larvae of Mesocestoides are rarely encountered in nonhuman primates, with most cases reported in baboons. Infection of macaques has been occasionally diagnosed, but Mesocestoides in the lung parenchyma is extremely rare. We have previously demonstrated that in macaques with terminal AIDS, simian immunodeficiency virus (SIV)-infected leukocytes are rarely found in cellular infiltrates associated with opportunistic infections or preexisting disease. Here we describe larvae (tetrathyridia) of the cestode Mesocestoides in the lung of an adult, pigtailed macaque (Macaca nemestrina) during acute SIV infection in which virus-positive cells are present within the cellular infiltrates. These results describe a rare parasitic disease in pigtailed macaques and demonstrate that lentivirus-infected leukocytes can be associated with inflammatory sites during acute infection.     

Historical biogeography of an Indo‐Pacific passerine bird family (Pachycephalidae): different colonization patterns in the Indonesian and Melanesian archipelagos

Aim We use molecular‐based phylogenetic methods and ancestral area reconstructions to examine the systematic relationships and biogeographical history of the Indo‐Pacific passerine bird family Pachycephalidae (whistlers). Analysed within an explicit spatiotemporal framework, we elucidate distinct patterns of diversification across the Melanesian and Indonesian archipelagos and explore whether these results may be explained by regional palaeogeological events. We further assess the significance of upstream colonization and its role in species accumulation within the region. Location The Indo‐Pacific region, with an emphasis on the archipelagos on either side of the Australo‐Papuan continent. Methods We used three nuclear and two mitochondrial markers to construct a molecular phylogenetic hypothesis of the Pachycephalidae by analysing 35 of the 49 species known to belong to the family. The programs diva and Mr Bayes were used to reconstruct ancestral area relationships and to examine biogeographical relationships across the family, and beast was implemented to assess the timing of dispersal events. Results We constructed a molecular phylogenetic hypothesis for the Pachycephalidae and estimated divergence times and ancestral area relationships. Different colonization patterns are apparent for the Pachycephalidae in the Indonesian and the Melanesian archipelagos. The Indonesian archipelago was colonized numerous times, whereas one or two colonizations of the Melanesian archipelagos account for the entire diversity of that region. After initial colonization of the Melanesian archipelagos some whistler species recolonized Australia and may have commenced a second round of colonization into Melanesia. Main conclusions The contrasting dispersal patterns of whistlers in archipelagos on either side of the Australo‐Papuan continent are congruent with the arrangement and history of islands in each of the regions and demonstrate that knowledge of palaeogeography is important for an understanding of evolutionary patterns in archipelagos. We also highlight that recolonization of continents from islands may be more common than has previously been assumed.     

Labile ecotypes accompany rapid cladogenesis in an adaptive radiation of Mandarina (Bradybaenidae) land snails

The endemic land snail genus Mandarina of the oceanic Bonin Islands shows exceptionally diverse morphological and ecological traits. Previous studies have already provided evidence that speciation on different islands of the three main archipelagos was such that similar ecotypes evolved independently in different lineages and islands. Here we present data to show that the same species can have different ecotypes. As most of the characters involved are inherited, then variation between ecotypes must represent genetic differences between populations. We then show that the radiation on the Bonin Islands is derived from a single colonization event, and use a mitochondrial phylogeny to provide evidence for a burst of cladogenesis soon after colonization. As divergent selection has previously been implicated in causing differences between Mandarina species, and theory predicts that most of the speciation should have taken place early in their history, then the study adds to the evidence for an adaptive radiation by ecological speciation in Mandarina . However, while the diversity of ecotypes present at each site is dependent on the regime of natural selection and competition, geography still must have an important role.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 269–282.     

The colonization of Scottish islands by the common shrew, Sorex araneus (Eulipotyphla: Soricidae)

In this paper we apply molecular methods to study the colonization of islands off the west coast of Scotland by the common shrew ( Sorex araneus L.), and current gene flow. We collected 497 individuals from 13 islands of the Inner Hebrides and Clyde Island groups and six mainland regions. Individuals were genotyped at eight microsatellite loci, and the mitochondrial cytochrome b sequence (1140 base pairs) was obtained for five individuals from each island/mainland region. Based on these molecular data, island colonization apparently proceeded directly from the mainland, except for Islay, for which Jura was the most likely source population. Raasay may also have been colonized by island hopping. Most island populations are genetically very distinct from the mainland populations, suggesting long periods of isolation. Two exceptions to this are the islands of Skye and Seil, which are geographically and genetically close to the mainland, suggesting in each case that there has been long-term gene flow between these islands and the mainland. We consider possible methods of island colonization, including human-mediated movement, swimming, and land and ice bridges.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 797–808.     

Modelling population persistence on islands: mammal introductions in the New Zealand archipelago

Islands are likely to differ in their susceptibility to colonization or invasion due to variation in factors that affect population persistence, including island area, climatic severity and habitat modification. We tested the importance of these factors in explaining the persistence of 164 introductions of six mammal species to 85 islands in the New Zealand archipelago using survival analysis and model selection techniques. As predicted by the theory of stochastic population growth, extinction risk was the greatest in the period immediately following introduction, declining rapidly to low probability by ca 25 years. This suggests that initially small populations were at greatest risk of extinction and that populations which survived for 25 years were likely to persist subsequently for much longer. Islands in the New Zealand archipelago become colder and windier with increasing latitude, and the probability of mammal populations persisting on islands declined steeply with increasing latitude. Hence, our results suggest that climatic suitability was an important determinant of the outcome of these invasions. The form of the relationship between latitude and persistence probability differed among species, emphasizing that the outcome of colonization attempts is species-environment specific.     

Northern pigtailed macaques rely on old growth plantations to offset low fruit availability in a degraded forest fragment

Space-use and foraging strategies are important facets to consider in regard to the ecology and conservation of primates. For this study, we documented movement, ranging, and foraging patterns of northern pigtailed macaques (Macaca leonina) for 14 months in a degraded habitat with old growth Acacia and Eucalyptus plantations at the Sakaerat Biosphere Reserve in northeastern Thailand. We used hidden Markov models and characteristic hull polygons to analyze these patterns in regard to fruit availability. Macaques' home range (HR) was 599 ha and spanned through a natural dry-evergreen forest (DEF), and plantation forest. Our results showed that active foraging increased with higher fruit availability in DEF. Macaques changed to a less continuous behavioral state during periods of lower fruit availability in DEF, repeatedly moving from foraging to transiting behavior, while extending their HR further into plantation forest and surrounding edge areas. Concomitantly, macaques shifted their diet from fleshy to dry fruit such as the introduced Acacia species. Our results showed that the diet and movement ecology adaptations of northern pigtailed macaques were largely dependent on availability of native fruits, and reflected a “high-cost, high-yield” foraging strategy when fresh food was scarce and dry fruit was available in plantation forest. Conversely, wild-feeding northern pigtailed macaque populations inhabiting pristine habitat approached a “low-cost, low-yield” foraging strategy. Our results outline the effects of habitat degradation on foraging strategies and show how a flexible species can cope with its nutritional requirements.     

Evolution in a tropical archipelago: comparative phylogeography of Philippine fauna and flora reveals complex patterns of colonization and diversification

An unusual geological setting and a high level of endemism makes the Philippine islands of great interest to biogeography. These islands lie adjacent to the continental (Sunda) shelf, yet the majority of the islands have never been directly attached to the mainland. Existing hypotheses of colonization and diversification processes have been tested across multiple taxa, but only in ahistorical contexts. We present explicit phylogenetic predictions based on these hypotheses, and then test them using new molecular datasets for four Philippine birds. Two proposed colonization routes to the northern Philippines (from mainland Asia and Palawan) are difficult to differentiate from each other, except on the basis of outgroup, as are the two routes from the south (Sulu archipelago and Sulawesi). We find unique colonization and diversification patterns for each taxon. These results contrast with expectations from Pleistocene geography, with Luzon and Mindoro indistinguishable genetically, and Negros and Panay are often nonsister taxa. Combining these data with a literature search for studies addressing these patterns, Philippine organisms shows some evidence for each proposed colonization route but the greatest support is for the two routes from Borneo. Many taxa exhibit multiple colonization events using several of these routes, contrasting with past assumptions of single colonization events. Island‐by‐island differentiation within the Philippines follows, with patterns reflecting colonization patterns rather than Pleistocene geography, particularly for highland species. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 620–639.     

Diversification of Sulawesi macaque monkeys: decoupled evolution of mitochondrial and autosomal DNA

Abstract. In macaque monkeys, females are philopatric and males are obligate dispersers. This social system is expected to differently affect evolution of genetic elements depending on their mode of inheritance. Because of this, the geographic structure of molecular variation may differ considerably in mitochondrial DNA (mtDNA) and in autosomal DNA (aDNA) in the same individuals, even though these genomes are partially co-inherited. On the Indonesian island of Sulawesi, macaque monkeys underwent an explosive diversification as a result of range fragmentation. Today, barriers to dispersal have receded and fertile hybrid individuals can be found at contact zones between parapatric species. In this study, we examine the impact of range fragmentation on Sulawesi macaque mtDNA and aDNA by comparing evolution, phylogeography, and population subdivision of each genome. Our results suggest that mtDNA is paraphyletic in some species, and that mtDNA phylogeography is largely consistent with a pattern of isolation by distance. Autosomal DNA, however, is suggestive of fragmentation, in that interspecific differentiation across most contact zones is significant but intraspecific differentiation between contact zones is not. Furthermore, in mtDNA, most molecular variation is partitioned between populations within species but in aDNA most variation is partitioned within populations. That mtDNA has a different geographic structure than aDNA (and morphology) in these primates is a probable consequence of (1) a high level of ancestral polymorphism in mtDNA, (2) differences between patterns of ancestral dispersal of matrilines and contemporary dispersal of males, and (3) the fact that female philopatry impedes gene flow of macaque mtDNA.     

MHC class I characterization of Indonesian cynomolgus macaques

Cynomolgus macaques (Macaca fascicularis) are quickly becoming a useful model for infectious disease and transplantation research. Even though cynomolgus macaques from different geographic regions are used for these studies, there has been limited characterization of full-length major histocompatibility complex (MHC) class I immunogenetics of distinct geographic populations. Here, we identified 48 MHC class I cDNA nucleotide sequences in eleven Indonesian cynomolgus macaques, including 41 novel Mafa-A and Mafa-B sequences. We found seven MHC class I sequences in Indonesian macaques that were identical to MHC class I sequences identified in Malaysian or Mauritian macaques. Sharing of nucleotide sequences between these geographically distinct populations is also consistent with the hypothesis that Indonesia was a source of the Mauritian macaque population. In addition, we found that the Indonesian cDNA sequence Mafa-B7601 is identical throughout its peptide binding domain to Mamu-B03, an allele that has been associated with control of Simian immunodeficiency virus (SIV) viremia in Indian rhesus macaques. Overall, a better understanding of the MHC class I alleles present in Indonesian cynomolgus macaques improves their value as a model for disease research, and it better defines the biogeography of cynomolgus macaques throughout Southeast Asia.