Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis)

The evolutionary mechanisms generating the tremendous biodiversity of islands have long fascinated evolutionary biologists. Genetic drift and divergent selection are predicted to be strong on islands and both could drive population divergence and speciation. Alternatively, strong genetic drift may preclude adaptation. We conducted a genomic analysis to test the roles of genetic drift and divergent selection in causing genetic differentiation among populations of the island fox (Urocyon littoralis). This species consists of six subspecies, each of which occupies a different California Channel Island. Analysis of 5293 SNP loci generated using Restriction‐site Associated DNA (RAD) sequencing found support for genetic drift as the dominant evolutionary mechanism driving population divergence among island fox populations. In particular, populations had exceptionally low genetic variation, small N_e (range = 2.1–89.7; median = 19.4), and significant genetic signatures of bottlenecks. Moreover, islands with the lowest genetic variation (and, by inference, the strongest historical genetic drift) were most genetically differentiated from mainland grey foxes, and vice versa, indicating genetic drift drives genome‐wide divergence. Nonetheless, outlier tests identified 3.6–6.6% of loci as high F_ST outliers, suggesting that despite strong genetic drift, divergent selection contributes to population divergence. Patterns of similarity among populations based on high F_ST outliers mirrored patterns based on morphology, providing additional evidence that outliers reflect adaptive divergence. Extremely low genetic variation and small N_e in some island fox populations, particularly on San Nicolas Island, suggest that they may be vulnerable to fixation of deleterious alleles, decreased fitness and reduced adaptive potential.     

Selection and geographic isolation influence hummingbird speciation: genetic, acoustic and morphological divergence in the wedge-tailed sabrewing (Campylopterus curvipennis)

Background  

Mesoamerica is one of the most threatened biodiversity hotspots in the world, yet we are far from understanding the geologic history and the processes driving population divergence and speciation for most endemic taxa. In species with highly differentiated populations selective and/or neutral factors can induce rapid changes to traits involved in mate choice, promoting reproductive isolation between allopatric populations that can eventually lead to speciation. We present the results of genetic differentiation, and explore drift and selection effects in promoting acoustic and morphological divergence among populations of Campylopterus curvipennis, a lekking hummingbird with an extraordinary vocal variability across Mesoamerica.     

Spatial and ecological population genetic structures within two island‐endemic Aeonium species of different niche width

The Crassulacean genus Aeonium is a well‐known example for plant species radiation on oceanic archipelagos. However, while allopatric speciation among islands is documented for this genus, the role of intra‐island speciation due to population divergence by topographical isolation or ecological heterogeneity has not yet been addressed. The aim of this study was to investigate intraspecific genetic structures and to identify spatial and ecological drivers of genetic population differentiation on the island scale. We analyzed inter simple sequence repeat variation within two island‐endemic Aeonium species of La Palma: one widespread generalist that covers a large variety of different habitat types (Ae. davidbramwellii) and one narrow ecological specialist (Ae. nobile), in order to assess evolutionary potentials on this island. Gene pool differentiation and genetic diversity patterns were associated with major landscape structures in both species, with phylogeographic implications. However, overall levels of genetic differentiation were low. For the generalist species, outlier loci detection and loci–environment correlation approaches indicated moderate signatures of divergent selection pressures linked to temperature and precipitation variables, while the specialist species missed such patterns. Our data point to incipient differentiation among populations, emphasizing that ecological heterogeneity and topographical structuring within the small scales of an island can foster evolutionary processes. Very likely, such processes have contributed to the radiation of Aeonium on the Canary Islands. There is also support for different evolutionary mechanisms between generalist and specialist species.     

Genetic diversity and colony structure of Tapinoma melanocephalum on the islands and mainland of South China

Aim

Tapinoma melanocephalum is listed as one of the most important invasive pest species in China. Information regarding the patterns of invasion and effects of geographic isolation on the population genetics of this species is largely lacking.

Location

South China.

Methods

To address this problem, we genotyped 39 colonies (two colonies were collapsed due to genetic similarity) using microsatellite markers and mitochondrial DNA sequencing to compare colony genetic structure of T. melanocephalum on the mainland and islands of South China.

Results

An analysis of the colony genotypes showed that the genetic diversity of the mainland population was slightly higher than that of the island populations but not significantly so. However, the observed heterozygosity on Shangchuan Island (SCD) was significantly lower than that of the other colonies. We also found six haplotypes in 111 mitochondrial DNA COI sequences. The relatedness (r) value between colonies of SCD was 0.410, higher than that of the other populations. The genetic clusters among colonies were not related to geographic locations and exhibited admixture likely due to frequent human‐mediated dispersal associated with trade between the mainland population and the islands. Pairwise F_STs between populations showed differentiation among mainland populations, while SCD displayed high levels of divergence (F_ST > 0.15) from most mainland populations. There was no significant isolation by distance among colonies. Most populations showed signs of a bottleneck effect.

Main conclusions

Our study suggests that there was no significant difference in the genetic diversity among the islands and the mainland; however, the lower genetic diversity, the higher degree of genetic divergence from other colonies, and the higher relatedness among nestmates made the SCD population stand out from all the others.     

Genetic structure among Charadrius plovers on the African mainland and islands of Madagascar and St Helena

Colonization of islands by long-distance dispersers has great impact on genetic diversification among populations and may spearhead speciation events. We investigated intra- and interspecific divergence in Charadrius plovers with populations on mainland Africa, Madagascar and St Helena. We analysed microsatellite loci and sequence data from four nuclear and two mitochondrial gene regions. Charadrius plovers are shorebirds with high dispersal and mobility. Our results confirmed genetic differentiation between Madagascar and mainland populations of three plover species (White-fronted Plover Charadrius marginatus, Kittlitz's Plover Charadrius pecuarius and, based on sequence data only, Three-banded Plover Charadrius tricollaris) but highlight substantial variation in levels of intraspecific divergence among the three species. Namely, the Kittlitz's Plover, a dispersive habitat generalist with a polygamous mating system, exhibited lower island–mainland differentiation (0.05% COI sequence divergence) compared with the two monogamous species, the White-fronted Plover (0.6% COI divergence) and Three-banded Plover (1.6% COI divergence). In addition, past colonization of the islands of St Helena and Madagascar by ancestors of today's Kittlitz's Plover has led to the evolution of two endemic island species, the Madagascar Plover Charadrius thoracicus and the more closely-related St Helena Plover Charadrius sanctaehelenae. We discuss the factors driving species differences in island–mainland divergence and highlight the importance of conserving genetically unique island populations and island habitats to safeguard future evolutionary potential.     

Evolutionary history of the endangered fish <Emphasis Type="Italic">Zoogoneticus quitzeoensis</Emphasis>(Bean, 1898) (Cyprinodontiformes: Goodeidae) using a sequential approach to phylogeography based on mitochondrial and nuclear DNA data

Background  

Tectonic, volcanic and climatic events that produce changes in hydrographic systems are the main causes of diversification and speciation of freshwater fishes. Elucidate the evolutionary history of freshwater fishes permits to infer theories on the biotic and geological evolution of a region, which can further be applied to understand processes of population divergence, speciation and for conservation purposes. The freshwater ecosystems in Central Mexico are characterized by their genesis dynamism, destruction, and compartmentalization induced by intense geologic activity and climatic changes since the early Miocene. The endangered goodeid Zoogoneticus quitzeoensis is widely distributed across Central México, thus making it a good model for phylogeographic analyses in this area.     

Combined next‐generation sequencing and morphology reveal fine‐scale speciation in Crocodile Skinks (Squamata: Scincidae: Tribolonotus)

Next‐generation sequencing has vast potential to revolutionize the fields of phylogenetics and population genetics through its ability to collect genomic scale data sets of thousands of orthologous loci. Despite this potential, other types of data (e.g. morphology, ecology) remain important, particularly for studies endeavouring to delimit species. Here, we integrate next‐generation sequencing with morphology to examine divergence between populations of Tribolonotus pseudoponceleti on the islands of Buka and Bougainville in the Solomon Archipelago. We used the Ion Torrent PGM to collect over 648 Mbp of sequence data for 12 samples, representing 1526 loci recovered from all samples, and 3342 were recovered from at least six samples. Genetic structure analyses strongly support the distinctiveness of these two populations, and Bayes factor delimitations decisively select speciation between Buka and Bougainville. Principal components and discriminant function analyses reveal concordant morphological divergence. Finally, demographic analyses via diffusion approximation and approximate Bayesian computation prefer a complex model of mid‐Pleistocene divergence with migration, and a later decrease or cessation of migration and population size shift, suggesting a scenario in which migration was enabled by Pleistocene merging of these two islands, and limited when isolated by higher sea levels. Further analysis of four Sanger sequenced loci in IMa2 had limited power to distinguish among models including and excluding migration, but resulted in similar population size and divergence time estimates, although with much broader confidence intervals. This study represents a framework for how next‐generation sequencing and morphological data can be combined and leveraged towards validating putative species and testing demographic scenarios for speciation.     

Complex inter‐island colonization and peripatric founder speciation promote diversification of flightless Pachyrhynchus weevils in the Taiwan–Luzon volcanic belt

Aim

We investigated the spatial and temporal patterns of diversification among colourful and flightless weevils, the Pachyrhynchus orbifer complex, to test the stepping‐stone hypothesis of colonization across the Taiwan–Luzon volcanic belt.

Location

Southeast Asia.

Methods

The phylogeny of the P. orbifer complex was reconstructed from a multi‐locus data set of mitochondrial and nuclear genes using maximum likelihood in RAxML and Bayesian inference in MRBAYES. Likelihood‐based tests in CONSEL were used to evaluate alternative tree topologies. Divergence times were estimated in beast based on a range of mutation rates. Ancestral range and biogeographical history were reconstructed using Bayesian binary MCMC (BBM) methods in RASP and in BioGeoBEARS. Demographic histories were inferred using the extended Bayesian skyline plot (EBSP). Species boundaries were tested using BPP.

Results

The phylogeny of the P. orbifer complex indicated strong support for seven reciprocally monophyletic lineages grouped by current island boundaries (Camiguin, Fuga, Dalupiri, Calayan, Babuyan, Orchid and Yaeyama Islands), except for a sister Green + Itbayat lineage. Complex and stochastic colonization of P. orbifer was inferred to have involved both northward and southward directions with short‐ and long‐distance dispersal events, which are strongly inconsistent with the strict stepping‐stone hypothesis. Divergence time estimates for all extant island lineages (<1 Myr of Middle Pleistocene) are much more recent than the geological ages (22.4–1.7 Myr) and subaerial existence (c. 3 Myr) of the islands. The statistically delimited seven cryptic species imply that the diversity of Pachyrhynchus from small peripheral islands continues to be largely under‐estimated.

Main conclusions

The non‐linear, more complex spatial and temporal settings of the archipelago and stochastic dispersal were probable key factors shaping the colonization history of the P. orbifer complex. Speciation of the P. orbifer complex may have occurred only between islands, indicating that peripatric speciation through the founders of stochastic dispersals was the major evolutionary driver.     

Towards a more general species–area relationship: diversity on all islands, great and small

Aim

To demonstrate a new and more general model of the species–area relationship that builds on traditional models, but includes the provision that richness may vary independently of island area on relatively small islands (the small island effect).

Location

We analysed species–area patterns for a broad diversity of insular biotas from aquatic and terrestrial archipelagoes.

Methods

We used breakpoint or piecewise regression methods by adding an additional term (the breakpoint transformation) to traditional species–area models. The resultant, more general, species–area model has three readily interpretable, biologically relevant parameters: (1) the upper limit of the small island effect (SIE), (2) an estimate of richness for relatively small islands and (3) the slope of the species–area relationship (in semi‐log or log–log space) for relatively large islands.

Results

The SIE, albeit of varying magnitude depending on the biotas in question, appeared to be a relatively common feature of the data sets we studied. The upper limit of the SIE tended to be highest for species groups with relatively high resource requirements and low dispersal abilities, and for biotas of more isolated archipelagoes.

Main conclusions

The breakpoint species–area model can be used to test for the significance, and to explore patterns of variation in small island effects, and to estimate slopes of the species–area (semi‐log or log–log) relationship after adjusting for SIE. Moreover, the breakpoint species–area model can be expanded to investigate three fundamentally different realms of the species–area relationship: (1) small islands where species richness varies independent of area, but with idiosyncratic differences among islands and with catastrophic events such as hurricanes, (2) islands beyond the upper limit of SIE where richness varies in a more deterministic and predictable manner with island area and associated, ecological factors and (3) islands large enough to provide the internal geographical isolation (large rivers, mountains and other barriers within islands) necessary for in situ speciation.

     

Local endemism and within‐island diversification of shrews illustrate the importance of speciation in building Sundaland mammal diversity

Island systems are important models for evolutionary biology because they provide convenient, discrete biogeographic units of study. Continental islands with a history of intermittent dry land connections confound the discrete definitions of islands and have led zoologists to predict (i) little differentiation of terrestrial organisms among continental shelf islands and (ii) extinction, rather than speciation, to be the main cause of differences in community composition among islands. However, few continental island systems have been subjected to well‐sampled phylogeographic studies, leaving these biogeographic assumptions of connectivity largely untested. We analysed nine unlinked loci from shrews of the genus Crocidura from seven mountains and two lowland localities on the Sundaic continental shelf islands of Sumatra and Java. Coalescent species delimitation strongly supported all currently recognized Crocidura species from Sumatra (six species) and Java (five species), as well as one undescribed species endemic to each island. We find that nearly all species of Crocidura in the region are endemic to a single island and several of these have their closest relative(s) on the same island. Intra‐island genetic divergence among allopatric, conspecific populations is often substantial, perhaps indicating species‐level diversity remains underestimated. One recent (Pleistocene) speciation event generated two morphologically distinct, syntopic species on Java, further highlighting the prevalence of within‐island diversification. Our results suggest that both between‐ and within‐island speciation processes generated local endemism in Sundaland, supplementing the traditional view that the region's fauna is relictual and primarily governed by extinction.     

Pherotypes are driving genetic differentiation within Streptococcus pneumoniae

Background  

The boundaries of bacterial species and the mechanisms underlying bacterial speciation are matters of intense debate. Theoretical studies have shown that recombination acts as a strong cohesive force preventing divergence in bacterial populations. Streptococcus pneumoniae populations have the telltale signs of high recombination with competence implicated as the major driving force behind gene exchange. Competence in S. pneumoniae is triggered by a quorum-sensing mechanism controlled by the competence-stimulating peptide pheromone.     

Two sisters in the same dress: <Emphasis Type="Italic">Heliconius</Emphasis> cryptic species

Background  

Sister species divergence and reproductive isolation commonly results from ecological adaptation. In mimetic Heliconius butterflies, shifts in colour pattern contribute to pre- and post-mating reproductive isolation and are commonly correlated with speciation. Closely related mimetic species are therefore not expected, as they should lack several important sources of reproductive isolation.     

Gene flow,linked selection,and divergent sorting of ancient polymorphism shape genomic divergence landscape in a group of edaphic specialists

Interpreting the formation of genomic variation landscape, especially genomic regions with elevated differentiation (i.e. islands), is fundamental to a better understanding of the genomic consequences of adaptation and speciation. Edaphic islands provide excellent systems for understanding the interplay of gene flow and selection in driving population divergence and speciation. However, discerning the relative contribution of these factors that modify patterns of genomic variation remains difficult. We analysed 132 genomes from five recently divergent species in Primulina genus, with four species distributed in Karst limestone habitats and the fifth one growing in Danxia habitats. We demonstrated that both gene flow and linked selection have contributed to genome-wide variation landscape, where genomic regions with elevated differentiation (i.e., islands) were largely derived by divergent sorting of ancient polymorphism. Specifically, we identified several lineage-specific genomic islands that might have facilitated adaptation of P. suichuanensis to Danxia habitats. Our study is amongst the first cases disentangling evolutionary processes that shape genomic variation of plant specialists, and demonstrates the important role of ancient polymorphism in the formation of genomic islands that potentially mediate adaptation and speciation of endemic plants in special soil habitats.     

Of mice and mammoths: generality and antiquity of the island rule

Aim

We assessed the generality of the island rule in a database comprising 1593 populations of insular mammals (439 species, including 63 species of fossil mammals), and tested whether observed patterns differed among taxonomic and functional groups.

Location

Islands world‐wide.

Methods

We measured museum specimens (fossil mammals) and reviewed the literature to compile a database of insular animal body size (S_i = mean mass of individuals from an insular population divided by that of individuals from an ancestral or mainland population, M). We used linear regressions to investigate the relationship between S_i and M, and ANCOVA to compare trends among taxonomic and functional groups.

Results

S_i was significantly and negatively related to the mass of the ancestral or mainland population across all mammals and within all orders of extant mammals analysed, and across palaeo‐insular (considered separately) mammals as well. Insular body size was significantly smaller for bats and insectivores than for the other orders studied here, but significantly larger for mammals that utilized aquatic prey than for those restricted to terrestrial prey.

Main conclusions

The island rule appears to be a pervasive pattern, exhibited by mammals from a broad range of orders, functional groups and time periods. There remains, however, much scatter about the general trend; this residual variation may be highly informative as it appears consistent with differences among species, islands and environmental characteristics hypothesized to influence body size evolution in general. The more pronounced gigantism and dwarfism of palaeo‐insular mammals, in particular, is consistent with a hypothesis that emphasizes the importance of ecological interactions (time in isolation from mammalian predators and competitors was 0.1 to > 1.0 Myr for palaeo‐insular mammals, but < 0.01 Myr for extant populations of insular mammals). While ecological displacement may be a major force driving diversification in body size in high‐diversity biotas, ecological release in species‐poor biotas often results in the convergence of insular mammals on the size of intermediate but absent species.     

Riding the Kuroshio Current: Stepping stone dispersal of the Okinawa tree lizard across the East Asian Island Arc

Aim

Located hundreds of kilometres offshore of continental mainland Asia, the extremely high level of land vertebrate endemism in the East Asian Island Arc provides an excellent opportunity to test hypotheses regarding biogeographic processes and speciation. In this study, we aim to test alternative explanations for lineage diversification (vicariance versus dispersal models), and further develop a temporal framework for diversification in our focal taxon, which is consistent with the known age of these islands. We achieve these tests by investigating the historical biogeography of the Okinawa tree lizard (Japalura polygonata), one of the few widely‐distributed reptiles across this archipelago.

Location

The East Asian Island Arc: (1) Central Ryukyu (Amami and Okinawa groups); (2) Southern Ryukyu (Miyako and Yaeyama groups); (3) Taiwan and adjacent islands.

Methods

A total of 246 tissues were sampled from 10 localities in the Ryukyu archipelago and 17 localities in Taiwan, covering the entire distributional range of this species, including all subspecies. DNA sequences of the mitochondrial cytochrome b, 16S ribosomal RNA, nuclear BACH‐1 and RAG‐1 genes (total: 4,684 bp) were obtained from these samples. We used maximum likelihood and Bayesian methods to infer phylogeny and divergence time, and used a model‐fitting method of biogeographical inference to estimate ancestral range evolution.

Results

Multiple lines of evidence combine to identify a general pattern of dispersal‐mediated diversification northward through the archipelago, following initial dispersal from Taiwan. These included (1) a phylogenetic estimate, revealing a sequential, south‐to‐north branching pattern; (2) ancestral range estimation, inferring multiple overseas dispersals and subsequent colonization of new landmasses; and (3) a reduction in genetic variation observed in successively‐diverging lineages, decreasing from Taiwan northward, towards more remote islands. These results provide strong statistical support for an interpretation of successive bouts of dispersal via the powerful, well‐documented, south‐to‐north Kuroshio Current. Estimation of divergence times suggests that most clades in southern Ryukyu and Taiwan diverged early, giving rise to lineages that have remained isolated, and that more recently‐diverged lineages then colonized northward to subsequently occupy the landmasses of the Central Ryukyu archipelago.

Main conclusions

Our general inference of biogeographic history in Japalura polygonata suggested that this species originated on Taiwan and the Yaeyama group, and arrived at its current distribution in Miyako, Okinawa, Toku and Amami islands by a series of stepping‐stone dispersals, which we report for the first time for a terrestrial vertebrate endemic to this region.     

Phylogeography and allopatric divergence of cypress species (<Emphasis Type="Italic">Cupressus</Emphasis> L.) in the Qinghai-Tibetan Plateau and adjacent regions

Background  

Although allopatric speciation is viewed as the most common way in which species originate, allopatric divergence among a group of closely related species has rarely been examined at the population level through phylogeographic analysis. Here we report such a case study on eight putative cypress (Cupressus) species, which each have a mainly allopatric distribution in the Qinghai-Tibetan Plateau (QTP) and adjacent regions. The analysis involved sequencing three plastid DNA fragments (trnD-trnT, trnS-trnG and trnL-trnF) in 371 individuals sampled from populations at 66 localities.     

An “omics” approach to bridge community ecology and island biogeography

Understanding the dynamics of communities in space and time requires reconciling ecological and evolutionary processes, including colonization, adaptation, speciation and extinction. In practice, this has been challenging because empirical data obtained by traditional methods and predictive models typically focus on particular processes driving local community assembly and biogeographical structure. In this issue of Molecular Ecology, by using phylogenomics, population genomics and phenomics approaches, Darwell et al. show that ant community assembly on islands is governed by predictable eco‐evolutionary trends of geographical range expansion, adaptive radiation and local population decline. The authors provide one of the most robust lines of evidence that the evolutionary progression of island communities may often be directional and repeatable, as predicted by the concept of taxon cycles.     

Genetic population structure of sympatric and allopatric populations of Baltic ciscoes (<Emphasis Type="Italic">Coregonus albula</Emphasis>complex,Teleostei, Coregonidae)

Background  

Teleost fishes of the Coregonidae are good model systems for studying postglacial evolution, adaptive radiation and ecological speciation. Of particular interest is whether the repeated occurrence of sympatric species pairs results from in-situ divergence from a single lineage or from multiple invasions of one or more different lineages. Here, we analysed the genetic structure of Baltic ciscoes (Coregonus albula complex), examining 271 individuals from 8 lakes in northern Germany using 1244 polymorphic AFLP loci. Six lakes had only one population of C. albula while the remaining two lakes had C. albula as well as a sympatric species (C. lucinensis or C. fontanae).     

Evidence for divergent selection between the molecular forms of <Emphasis Type="Italic">Anopheles gambiae</Emphasis>: role of predation

Background  

The molecular forms of Anopheles gambiae are undergoing speciation. They are characterized by a strong assortative mating and they display partial habitat segregation. The M form is mostly found in flooded/irrigated areas whereas the S form dominates in the surrounding areas, but the ecological factors that shape this habitat segregation are not known. Resource competition has been demonstrated between species undergoing divergent selection, but resource competition is not the only factor that can lead to divergence.     

Evolution of male genitalia: environmental and genetic factors affect genital morphology in two <Emphasis Type="Italic">Drosophila</Emphasis> sibling species and their hybrids

Background  

The rapid evolution of genital morphology is a fascinating feature that accompanies many speciation events. However, the underlying patterns and explanatory processes remain to be settled. In this work we investigate the patterns of intraspecific variation and interspecific divergence in male genitalic morphology (size and shape) in the cactophilic sibling species Drosophila buzzatii and D. koepferae. Genital morphology in interspecific hybrids was examined and compared to the corresponding parental lines.