Importance of genetic drift during Pleistocene divergence as revealed by analyses of genomic variation

Determining what factors affect the structuring of genetic variation is key to deciphering the relative roles of different evolutionary processes in species differentiation. Such information is especially critical to understanding how the frequent shifts and fragmentation of species distributions during the Pleistocene translates into species differences, and why the effect of such rapid climate change on patterns of species diversity varies among taxa. Studies of mitochondrial DNA (mtDNA) have detected significant population structure in many species, including those directly impacted by the glacial cycles. Yet, understanding the ultimate consequence of such structure, as it relates to how species divergence occurs, requires demonstration that such patterns are also shared with genomic patterns of differentiation. Here we present analyses of amplified fragment length polymorphisms (AFLPs) in the montane grasshopper Melanoplus oregonensis to assess the evolutionary significance of past demographic events and associated drift-induced divergence as inferred from mtDNA. As an inhabitant of the sky islands of the northern Rocky Mountains, this species was subject to repeated and frequent shifts in species distribution in response to the many glacial cycles. Nevertheless, significant genetic structuring of M. oregonensis is evident at two different geographic and temporal scales: recent divergence associated with the recolonization of the montane meadows in individual sky islands, as well as older divergence associated with displacements into regional glacial refugia. The genomic analyses indicate that drift-induced divergence, despite the lack of long-standing geographic barriers, has significantly contributed to species divergence during the Pleistocene. Moreover, the finding that divergence associated with past demographic events involves the repartitioning of ancestral variation without significant reductions of genomic diversity has intriguing implications - namely, the further amplification of drift-induced divergence by selection.     

Landscape heterogeneity and local adaptation define the spatial genetic structure of Pacific salmon in a pristine environment

Identifying the spatial distribution of genetic variation across the landscape is an essential step in informing species conservation. Comparison of closely related and geographically overlapping species can be particularly useful in cases where landscape may similarly influence genetic structure. Congruent patterns among species highlight the importance that landscape heterogeneity plays in determining genetic structure whereas contrasting patterns emphasize differences in species-specific ecology and life-history or the importance of species-specific adaptation to local environments. We examined the interacting roles of demography and adaptation in determining spatial genetic structure in two closely related and geographically overlapping species in a pristine environment. Using single nucleotide polymorphism (SNP) loci exhibiting both neutral and putative adaptive variation, we evaluated the genetic structure of sockeye salmon in the Copper River, Alaska; these data were compared to existing data for Chinook salmon from the same region. Overall, both species exhibited patterns of isolation by distance; the spatial distribution of populations largely determined the distribution of genetic variation across the landscape. Further, both species exhibited largely congruent patterns of within- and among-population genetic diversity, highlighting the role that landscape heterogeneity and historical processes play in determining spatial genetic structure. Potential adaptive differences among geographically proximate sockeye salmon populations were observed when high F_ST outlier SNPs were evaluated in a landscape genetics context. Results were evaluated in the context of conservation efforts with an emphasis on reproductive isolation, historical processes, and local adaptation.     

Anagenetic evolution in island plants

Aim  Plants in islands have often evolved through adaptive radiation, providing the classical model of evolution of closely related species each with strikingly different morphological and ecological features and with low levels of genetic divergence. We emphasize the importance of an alternative (anagenetic) model of evolution, whereby a single island endemic evolves from a progenitor and slowly builds up genetic variation through time.
Location  Continental and oceanic islands.
Methods  We surveyed 2640 endemic angiosperm species in 13 island systems of the world, both oceanic and continental, for anagenetic and cladogenetic patterns of speciation. Genetic data were evaluated from a progenitor and derivative species pair in Ullung Island, Korea, and Japan.
Results  We show that the anagenetic model of evolution is much more important in oceanic islands than previously believed, accounting for levels of endemic specific diversity from 7% in the Hawaiian Islands to 88% in Ullung Island, Korea, with a mean for all islands of 25%. Examination of an anagenetically derived endemic species in Ullung Island reveals genetic (amplified fragment length polymorphism) variation equal or nearly equal to that of its continental progenitor.
Main conclusions  We hypothesize that, during anagenetic speciation, initial founder populations proliferate, and then accumulate genetic variation slowly through time by mutation and recombination in a relatively uniform environment, with drift and/or selection yielding genetic and morphological divergence sufficient for the recognition of new species. Low-elevation islands with low habitat heterogeneity are highly correlated with high levels of anagenetic evolution, allowing prediction of levels of the two models of evolution from these data alone. Both anagenetic and adaptive radiation models of speciation are needed to explain the observed levels of specific and genetic diversity in oceanic islands.     

Population expansion, isolation and selection: novel insights on the evolution of color diversity in the strawberry poison frog

The evolutionary mechanisms causing intraspecific diversity in aposematic color and pattern remain enigmatic. The strawberry poison frog (Oophaga pumilio) has diversified into a broad array of colors that span the visible spectrum. The most divergent phenotypes of O. pumilio are restricted to separate islands in the Bocas del Toro archipelago in western Panama, whereas throughout the majority of its range (from Nicaragua to western Panama) this species exhibits a single red phenotype. During the Holocene, sea-levels increased and changes in climate caused shifts in habitat through time. In the Bocas del Toro archipelago, rising sea-levels isolated previously connected populations in higher elevation habitats (forming islands). In this study we use historic measures of demography, ancestral distribution estimates, spatiotemporally explicit demographic models and genetic simulations to investigate the genetic consequences of the isolation due to sea-level changes and demographic processes mediated by recent climatic fluctuations. We then evaluate the role of these factors in the evolution of color in O. pumilio by measuring and comparing the deep coalescence of a neutrally evolving nuclear gene and a hypothetical autosomal coloration gene. Our results support a major role for recent population expansion and reduced gene flow (from isolation on islands) in the diversification of color across populations.     

Species Differentiation on a Dynamic Landscape: Shifts in Metapopulation Genetic Structure Using the Chronology of the Hawaiian Archipelago

Species formation during adaptive radiation often occurs in the context of a changing environment. The establishment and arrangement of populations, in space and time, sets up ecological and genetic processes that dictate the rate and pattern of differentiation. Here, we focus on how a dynamic habitat can affect genetic structure, and ultimately, differentiation among populations. We make use of the chronology and geographical history provided by the Hawaiian archipelago to examine the initial stages of population establishment and genetic divergence. We use data from a set of 6 spider lineages that differ in habitat affinities, some preferring low elevation habitats with a longer history of connection, others being more specialized for high elevation and/or wet forest, some with more general habitat affinities. We show that habitat preferences associated with lineages are important in ecological and genetic structuring. Lineages that have more restricted habitat preferences are subject to repeated episodes of isolation and fragmentation as a result of lava flows and vegetation succession. The initial dynamic set up by the landscape translates over time into discrete lineages. Further work is needed to understand how genetic changes interact with a changing set of ecological interactions amongst a shifting mosaic of landscapes to achieve species formation.     

THE EVOLUTIONARY HISTORY OF DARWIN'S FINCHES: SPECIATION,GENE FLOW,AND INTROGRESSION IN A FRAGMENTED LANDSCAPE

Many classic examples of adaptive radiations take place within fragmented systems such as islands or mountains, but the roles of mosaic landscapes and variable gene flow in facilitating species diversification is poorly understood. Here we combine phylogenetic and landscape genetic approaches to understand diversification in Darwin's finches, a model adaptive radiation. We combined sequence data from 14 nuclear introns, mitochondrial markers, and microsatellite variation from 51 populations of all 15 recognized species. Phylogenetic species‐trees recovered seven major finch clades: ground, tree, vegetarian, Cocos Island, grey and green warbler finches, and a distinct clade of sharp‐beaked ground finches (Geospiza cf. difficilis) basal to all ground and tree finches. The ground and tree finch clades lack species‐level phylogenetic structure. Interisland gene flow and interspecies introgression vary geographically in predictable ways. First, several species exhibit concordant patterns of population divergence across the channel separating the Galápagos platform islands from the separate volcanic province of northern islands. Second, peripheral islands have more admixed populations while central islands maintain more distinct species boundaries. This landscape perspective highlights a likely role for isolation of peripheral populations in initial divergence, and demonstrates that peripheral populations may maintain genetic diversity through outbreeding during the initial stages of speciation.     

Fungal communities living within leaves of native Hawaiian dicots are structured by landscape‐scale variables as well as by host plants

A phylogenetically diverse array of fungi live within healthy leaf tissue of dicotyledonous plants. Many studies have examined these endophytes within a single plant species and/or at small spatial scales, but landscape‐scale variables that determine their community composition are not well understood, either across geographic space, across climatic conditions, or in the context of host plant phylogeny. Here, we evaluate the contributions of these variables to endophyte beta diversity using a survey of foliar endophytic fungi in native Hawaiian dicots sampled across the Hawaiian archipelago. We used Illumina technology to sequence fungal ITS1 amplicons to characterize foliar endophyte communities across five islands and 80 host plant genera. We found that communities of foliar endophytic fungi showed strong geographic structuring between distances of 7 and 36 km. Endophyte community structure was most strongly associated with host plant phylogeny and evapotranspiration, and was also significantly associated with NDVI, elevation and solar radiation. Additionally, our bipartite network analysis revealed that the five islands we sampled each harboured significantly specialized endophyte communities. These results demonstrate how the interaction of factors at large and small spatial and phylogenetic scales shapes fungal symbiont communities.     

Patterns of genetic variability and habitat occupancy in Crepis triasii (Asteraceae) at different spatial scales: insights on evolutionary processes leading to diversification in continental islands

Background and Aims

Archipelagos are unique systems for studying evolutionary processes promoting diversification and speciation. The islands of the Mediterranean basin are major areas of plant richness, including a high proportion of narrow endemics. Many endemic plants are currently found in rocky habitats, showing varying patterns of habitat occupancy at different spatial scales throughout their range. The aim of the present study was to understand the impact of varying patterns of population distribution on genetic diversity and structure to shed light on demographic and evolutionary processes leading to population diversification in Crepis triasii, an endemic plant from the eastern Balearic Islands.

Methods

Using allozyme and chloroplast markers, we related patterns of genetic structure and diversity to those of habitat occupancy at a regional (between islands and among populations within islands) and landscape (population size and connectivity) scale.

Key Results

Genetic diversity was highly structured both at the regional and at the landscape level, and was positively correlated with population connectivity in the landscape. Populations located in small isolated mountains and coastal areas, with restricted patterns of regional occupancy, were genetically less diverse and much more differentiated. In addition, more isolated populations had stronger fine-scale genetic structure than well-connected ones. Changes in habitat availability and quality arising from marine transgressions during the Quaternary, as well as progressive fragmentation associated with the aridification of the climate since the last glaciation, are the most plausible factors leading to the observed patterns of genetic diversity and structure.

Conclusions

Our results emphasize the importance of gene flow in preventing genetic erosion and maintaining the evolutionary potential of populations. They also agree with recent studies highlighting the importance of restricted gene flow and genetic drift as drivers of plant evolution in Mediterranean continental islands.     

Genetic drift and rapid evolution of viviparity in insular fire salamanders (Salamandra salamandra)

Continental islands offer an excellent opportunity to investigate adaptive processes and to time microevolutionary changes that precede macroevolutionary events. We performed a population genetic study of the fire salamander (Salamandra salamandra), a species that displays unique intraspecific diversity of reproductive strategies, to address the microevolutionary processes leading to phenotypic and genetic differentiation of island, coastal and interior populations. We used eight microsatellite markers to estimate genetic diversity, population structure and demographic parameters in viviparous insular populations and ovoviviparous coastal and interior populations. Our results show considerable genetic differentiation (F(ST) range: 0.06-0.27), and no clear signs of gene flow among populations, except between the large and admixed interior populations. We find no support for island colonization by rafting or intentional/accidental anthropogenic introductions, indicating that rising sea levels were responsible for isolation of the island populations approximately 9000 years ago. Our study provides evidence of rapid genetic differentiation between island and coastal populations, and rapid evolution of viviparity driven by climatic selective pressures on island populations, geographic isolation with genetic drift, or a combination of these factors. Studies of these viviparous island populations in early stages of divergence help us better understand the microevolutionary processes involved in rapid phenotypic shifts.     

Genetic implications of bottleneck effects of differing severities on genetic diversity in naturally recovering populations: An example from Hawaiian coot and Hawaiian gallinule

The evolutionary trajectory of populations through time is influenced by the interplay of forces (biological, evolutionary, and anthropogenic) acting on the standing genetic variation. We used microsatellite and mitochondrial loci to examine the influence of population declines, of varying severity, on genetic diversity within two Hawaiian endemic waterbirds, the Hawaiian coot and Hawaiian gallinule, by comparing historical (samples collected in the late 1800s and early 1900s) and modern (collected in 2012–2013) populations. Population declines simultaneously experienced by Hawaiian coots and Hawaiian gallinules differentially shaped the evolutionary trajectory of these two populations. Within Hawaiian coot, large reductions (between −38.4% and −51.4%) in mitochondrial diversity were observed, although minimal differences were observed in the distribution of allelic and haplotypic frequencies between sampled time periods. Conversely, for Hawaiian gallinule, allelic frequencies were strongly differentiated between time periods, signatures of a genetic bottleneck were detected, and biases in means of the effective population size were observed at microsatellite loci. The strength of the decline appears to have had a greater influence on genetic diversity within Hawaiian gallinule than Hawaiian coot, coincident with the reduction in census size. These species exhibit similar life history characteristics and generation times; therefore, we hypothesize that differences in behavior and colonization history are likely playing a large role in how allelic and haplotypic frequencies are being shaped through time. Furthermore, differences in patterns of genetic diversity within Hawaiian coot and Hawaiian gallinule highlight the influence of demographic and evolutionary processes in shaping how species respond genetically to ecological stressors.     

Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae)

The endemic Hawaiian lobeliads are exceptionally species rich and exhibit striking diversity in habitat, growth form, pollination biology and seed dispersal, but their origins and pattern of diversification remain shrouded in mystery. Up to five independent colonizations have been proposed based on morphological differences among extant taxa. We present a molecular phylogeny showing that the Hawaiian lobeliads are the product of one immigration event; that they are the largest plant clade on any single oceanic island or archipelago; that their ancestor arrived roughly 13 Myr ago; and that this ancestor was most likely woody, wind-dispersed, bird-pollinated, and adapted to open habitats at mid-elevations. Invasion of closed tropical forests is associated with evolution of fleshy fruits. Limited dispersal of such fruits in wet-forest understoreys appears to have accelerated speciation and led to a series of parallel adaptive radiations in Cyanea, with most species restricted to single islands. Consistency of Cyanea diversity across all tall islands except Hawai ;i suggests that diversification of Cyanea saturates in less than 1.5 Myr. Lobeliad diversity appears to reflect a hierarchical adaptive radiation in habitat, then elevation and flower-tube length, and provides important insights into the pattern and tempo of diversification in a species-rich clade of tropical plants.     

Patterns of genetic diversity in the polymorphic ground snake (Sonora semiannulata)

We evaluated the genetic diversity of a snake species with color polymorphism to understand the evolutionary processes that drive genetic structure across a large geographic region. Specifically, we analyzed genetic structure of the highly polymorphic ground snake, Sonora semiannulata, (1) among populations, (2) among color morphs (3) at regional and local spatial scales, using an amplified fragment length polymorphism dataset and multiple population genetic analyses, including F_ST-based and clustering analytical techniques. Based upon these methods, we found that there was moderate to low genetic structure among populations. However, this diversity was not associated with geographic locality at either spatial scale. Similarly, we found no evidence for genetic divergence among color morphs at either spatial scale. These results suggest that despite dramatic color polymorphism, this phenotypic diversity is not a major driver of genetic diversity within or among populations of ground snakes. We suggest that there are two mechanisms that could explain existing genetic diversity in ground snakes: recent range expansion from a genetically diverse founder population and current or recent gene flow among populations. Our findings have further implications for the types of color polymorphism that may generate genetic diversity in snakes.     

Applying landscape genetics to the microbial world

Landscape genetics, which explicitly quantifies landscape effects on gene flow and adaptation, has largely focused on macroorganisms, with little attention given to microorganisms. This is despite overwhelming evidence that microorganisms exhibit spatial genetic structuring in relation to environmental variables. The increasing accessibility of genomic data has opened up the opportunity for landscape genetics to embrace the world of microorganisms, which may be thought of as ‘the invisible regulators’ of the macroecological world. Recent developments in bioinformatics and increased data accessibility have accelerated our ability to identify microbial taxa and characterize their genetic diversity. However, the influence of the landscape matrix and dynamic environmental factors on microorganism genetic dispersal and adaptation has been little explored. Also, because many microorganisms coinhabit or codisperse with macroorganisms, landscape genomic approaches may improve insights into how micro‐ and macroorganisms reciprocally interact to create spatial genetic structure. Conducting landscape genetic analyses on microorganisms requires that we accommodate shifts in spatial and temporal scales, presenting new conceptual and methodological challenges not yet explored in ‘macro’‐landscape genetics. We argue that there is much value to be gained for microbial ecologists from embracing landscape genetic approaches. We provide a case for integrating landscape genetic methods into microecological studies and discuss specific considerations associated with the novel challenges this brings. We anticipate that microorganism landscape genetic studies will provide new insights into both micro‐ and macroecological processes and expand our knowledge of species’ distributions, adaptive mechanisms and species’ interactions in changing environments.     

Disentangling the dynamics of invasive fireweed (<Emphasis Type="Italic">Senecio madagascariensis</Emphasis> Poir. species complex) in the Hawaiian Islands

Studies investigating the genetic variation of invasive species render opportunities to better understand the dynamics of biological invasions from an ecological and evolutionary perspective. In this study, we investigate fine-scale population genetic structure of invasive Senecio madagascariensis (fireweed) using microsatellite markers to determine levels of genetic diversity and how it pertains to introduction history of this species within and among the Hawaiian Islands. Dispersal patterns were interpreted and, together with a habitat suitability analysis, we aim to describe the potential range expansion of S. madgascariensis within the islands. Bayesian and frequency-based analyses revealed genetic structure with two major genetic demes corresponding to the two fireweed-infested islands of Maui and Hawaii. Both these demes showed further genetic sub-structure, each consisting of three genetically distinct subgroups. Overall, fireweed showed significant levels of inbreeding. Major genetic demes (Maui and Hawaii) differed in observed heterozygosities, inbreeding and genetic structure, each harbouring a large proportion of private alleles. In contrast to the current understanding of fireweed’s introduction history between the Hawaiian Islands, fine-scale population genetic parameters suggest that this species has been introduced at least twice, possibly even more, to the archipelago. Spatial analyses also revealed high correlation between genetic similarity and geographical proximity (>2 km apart) followed by a sharp decline. In addition, a single population was identified that likely resulted from a rare human- or animal-mediated extreme long-distance dispersal event from Maui to Hawaii. Bayesian and likelihood estimates of ‘first generation migrants’ also concurred that contemporary dispersal occurs more frequently over smaller spatial scales than larger scales. These findings indicate that spread in this species occurs primarily via a stratified strategy. Predictions from habitat suitability models indicate all Hawaiian Islands as highly suitable for fireweed invasion and the movement of propagules to currently uninfested islands and outlying suitable habitats should be avoided to circumvent further expansions of the invasion.     

Molecular phylogeny and adaptive radiation of the endemic Hawaiian Plantago species (Plantaginaceae)

Insular oceanic islands provide excellent opportunities for the study of evolutionary processes and adaptive radiation. The Hawaiian Plantago radiation comprises six endemic taxa showing considerable inter- and intraspecific morphological and ecological diversity. The rDNA internal (ITS) and external (ETS) transcribed spacers and two recently described chloroplast spacers, ndhF-rpl32 and rpl32-trnL, were sequenced to study phylogenetic relationships within this morphologically complex group. Phylogenetic analysis provided strong evidence for the monophyly of Hawaiian Plantago, suggesting that the lineage arose from a single long-distance dispersal event. Inconsistencies between nuclear and chloroplast phylogenies suggest a history of hybridization. The basal, unresolved dichotomy of the combined phylogeny is consistent with rapid phenotypic diversification of the major lineages early in the history of this group. Speciation has largely occurred allopatrically, with divergence a result of intraisland ecological shifts between bog and woodland habitats and interisland dispersal events. Most interisland colonizations were from older to younger islands with initial colonization of Kaua'i. In our analysis, P. pachyphylla is paraphyletic and taxonomic separation of the distinct morphotypes of this species appears justified. Furthermore, the apparent hybrid ancestry and unique morphology and habitat of the endangered P. princeps var. longibracteata support its recognition at the specific rank.     

A range-wide genetic bottleneck overwhelms contemporary landscape factors and local abundance in shaping genetic patterns of an alpine butterfly (Lepidoptera: Pieridae: Colias behrii)

Spatial and environmental heterogeneity are major factors in structuring species distributions in alpine landscapes. These landscapes have also been affected by glacial advances and retreats, causing alpine taxa to undergo range shifts and demographic changes. These nonequilibrium population dynamics have the potential to obscure the effects of environmental factors on the distribution of genetic variation. Here, we investigate how demographic change and environmental factors influence genetic variation in the alpine butterfly Colias behrii. Data from 14 microsatellite loci provide evidence of bottlenecks in all population samples. We test several alternative models of demography using approximate Bayesian computation (ABC), with the results favouring a model in which a recent bottleneck precedes rapid population growth. Applying independent calibrations to microsatellite loci and a nuclear gene, we estimate that this bottleneck affected both northern and southern populations 531–281 years ago, coinciding with a period of global cooling. Using regression approaches, we attempt to separate the effects of population structure, geographical distance and landscape on patterns of population genetic differentiation. Only 40% of the variation in F_ST is explained by these models, with geographical distance and least‐cost distance among meadow patches selected as the best predictors. Various measures of genetic diversity within populations are also decoupled from estimates of local abundance and habitat patch characteristics. Our results demonstrate that demographic change can have a disproportionate influence on genetic diversity in alpine species, contrasting with other studies that suggest landscape features control contemporary demographic processes in high‐elevation environments.     

Contrasting diversity and demographic signals in sympatric narrow‐range endemic shrubs of the south‐west Western Australian semi‐arid zone

Comparative studies of sympatric species that integrate both phylogeographical and population genetic approaches provide insight into how demographic events and life history traits shape adaptive potential and drive species persistence. Such studies are rare for species‐rich and strongly structured environments, especially those of the southern hemisphere. For two sympatric, perennial shrubs of the south‐west Western Australian semi‐arid zone, Grevillea globosa and Mirbelia sp. Bursarioides, we assessed historical and contemporary genetic diversity and structure, demographic processes and ratios of pollen to seed dispersal. Phylogeographical structure was not detected and haplotype networks were star‐like. Number of haplotypes, nucleotide diversity, haplotype diversity, and allelic diversity were statistically significantly lower for G. globosa than for M. sp. Bursarioides. Levels of haplotype divergence and more contemporary genetic divergence and expected heterozygosity were lower for G. globosa than for M. sp. Bursarioides, but differences were not statistically significant. Both species exhibited signals of isolation by distance and low pollen to seed dispersal ratios (5.26:1 and 6.88:1). Grevillea globosa displayed signals of historical and contemporary demographic expansion. Results imply an important role for aspects of seed ecology that impact population demography, as well as direct dispersal and a significant contribution of seed dispersal to genetic connectivity in a semi‐arid landscape.     

Spatially explicit models of dynamic histories: examination of the genetic consequences of Pleistocene glaciation and recent climate change on the American Pika

A central goal of phylogeography is to identify and characterize the processes underlying divergence. One of the biggest impediments currently faced is how to capture the spatiotemporal dynamic under which a species evolved. Here, we described an approach that couples species distribution models (SDMs), demographic and genetic models in a spatiotemporally explicit manner. Analyses of American Pika (Ochotona princeps) from the sky islands of the central Rocky Mountains of North America are used to provide insights into key questions about integrative approaches in landscape genetics, population genetics and phylogeography. This includes (i) general issues surrounding the conversion of time-specific SDMs into simple continuous, dynamic landscapes from past to current, (ii) the utility of SDMs to inform demographic models with deme-specific carrying capacities and migration potentials as well as (iii) the contribution of the temporal dynamic of colonization history in shaping genetic patterns of contemporary populations. Our results support that the inclusion of a spatiotemporal dynamic is an important factor when studying the impact of distributional shifts on patterns of genetic data. Our results also demonstrate the utility of SDMs to generate species-specific predictions about patterns of genetic variation that account for varying degrees of habitat specialization and life history characteristics of taxa. Nevertheless, the results highlight some key issues when converting SDMs for use in demographic models. Because the transformations have direct effects on the genetic consequence of population expansion by prescribing how habitat heterogeneity and spatiotemporal variation is related to the species-specific demographic model, it is important to consider alternative transformations when studying the genetic consequences of distributional shifts.