Divergent lineages in a young species: The case of datilillo (Yucca valida), a broadly distributed plant from the Baja California Peninsula.

PREMISE: Globally, barriers triggered by climatic changes have caused habitat fragmentation and population allopatric divergence. Across North America, oscillations during the Quaternary have played important roles in the distribution of wildlife. Notably, diverse plant species from the Baja California Peninsula in western North America, isolated during the Pleistocene glacial-interglacial cycles, exhibit strong genetic structure and highly concordant divergent lineages across their ranges. A representative plant genus of the peninsula is Yucca, with Y. valida having the widest range. Although a dominant species, it has an extensive distribution discontinuity between 26° N and 27° N, suggesting restricted gene flow. Moreover, historical distribution models indicate the absence of an area with suitable conditions for the species during the Last Interglacial, making it an interesting model for studying genetic divergence. METHODS: We assembled 4411 SNPs from 147 plants of Y. valida throughout its range to examine its phylogeography to identify the number of genetic lineages, quantify their genetic differentiation, reconstruct their demographic history and estimate the age of the species. RESULTS: Three allopatric lineages were identified based on the SNPs. Our analyses support that genetic drift is the driver of genetic differentiation among these lineages. We estimated an age of less than 1 million years for the common ancestor of Y. valida and its sister species. CONCLUSIONS: Habitat fragmentation caused by climatic changes, low dispersal, and an extensive geographical range gap acted as cumulative mechanisms leading to allopatric divergence in Y. valida.

Interspecific competitive interactions affect body size and oxidative status of two nonnative salmonid species.

In fish, interspecific interactions between nonnative and other sympatric species are considered determinants in shaping species assemblages. Such interactions can also arise between nonnative fish species only, including salmonids such as the brown trout (Salmo trutta, Linnaeus, 1758) and the rainbow trout (Oncorhynchus mykiss, Walbaum, 1792), returning contrasting outcomes. The present manipulative experiment was aimed at exploring the effect of interspecific competition on the body growth and the oxidative status of parr (2 + -year-old individuals) of the brown trout and the rainbow trout. Allopatric (intraspecific competition) and sympatric (interspecific competition) populations of these species were experimentally recreated in two wild streams. At the end of a 2-month-long experiment, changes in specific growth rate (SGR), oxidative status (i.e., levels of reactive oxygen species and activity of antioxidant enzymes such as superoxide dismutase - SOD, catalase - CAT and glutathione peroxidase - GPx) and oxidative damage (i.e., lipid peroxidation) were investigated in brown and rainbow trout individuals maintained in allopatric or sympatric populations. Sympatric interactions between rainbow and brown trout parr resulted in a significant decrease in SGR of brown trout individuals only. Moreover, an overall modulation of the oxidative status, in terms of an increase in ROS levels coupled with the activation of SOD and CAT activity, occurred in brown trout individuals under sympatric conditions. These findings might suggest that, under sympatric conditions, parr of the rainbow trout are more competitive than brown trout for food acquisition. However, this competition affected the antioxidant defenses of the brown trout only, probably because of reduced ingestion of dietary antioxidants or increased physical activity and aggressive behavior. Thus, interspecific interactions can induce physiological and phenotypic effects on parr of nonnative salmonids, with potential consequences on the establishment of populations of these species in freshwater ecosystems.

A unified evolutionary framework for understanding parasite infection and host migratory behaviour.

Animal migration impacts organismal health and parasite transmission: migrants are simultaneously exposed to parasites and able to reduce infection for both individuals and populations. However, these dynamics are difficult to study; empirical studies reveal disparate results while existing theory makes assumptions that simplify natural complexity. Here, we systematically review empirical studies of migration and infection across taxa, highlighting key gaps in our understanding. Next, we develop a unified evolutionary framework incorporating different selective pressures of parasite-migration interactions while accounting for ecological complexity that goes beyond previous theory. Our framework generates diverse migration-infection patterns paralleling those seen in empirical systems, including partial and differential migration. Finally, we generate predictions about which mechanisms dominate which empirical systems to guide future studies. Our framework provides an overarching understanding of selective pressures shaping migration patterns in the context of animal health and disease, which is critical for predicting how environmental change may threaten migration.

Isolation by resistance explains genetic diversity in the Arremon brushfinches of northern Mesoamerica.

Genetic differentiation between and within natural populations is the result of the joint effects of neutral and adaptative processes. In addition, the spatial arrangement of the landscape promotes connectivity or creates barriers to gene flow, directly affecting speciation processes. In this study, we carried out a landscape genomics analysis using NextRAD data from a montane forest specialist bird complex, the Mesoamerican Chestnut-capped/Green-striped Brushfinch of the genus Arremon. Specifically, we examined population genomic structure using different assignment methods and genomic differentiation and diversity, and we tested alternative genetic isolation hypotheses at the individual level (e.g., isolation by barrier, IBB; isolation by environment, IBE; isolation by resistance, IBR). We found well-delimited genomic structuring (K = 5) across Mesoamerican montane forests in the studied group. Individual-level genetic distances among major montane ranges were mainly explained by IBR hypotheses in this sedentary Neotropical taxon. Our results uncover genetic distances/differentiation and patterns of gene flow in allopatric species that support the role of tropical mountains as spatial landscape drivers of biodiversity. IBR clearly supports a pattern of conserved niche-tracking of suitable habitat conditions and topographic complexity throughout glacial-interglacial dynamics.

Morphological and environmental differentiation as prezygotic reproductive barriers between parapatric and allopatric Campanula rotundifolia agg. cytotypes.

BACKGROUND AND AIMS: Reproductive isolation and local establishment are necessary for plant speciation. Polyploidy, the possession of more than two complete chromosome sets, creates a strong postzygotic reproductive barrier between diploid and tetraploid cytotypes. However, this barrier weakens between polyploids (e.g. tetraploids and hexaploids). Reproductive isolation may be enhanced by cytotype morphological and environmental differentiation. Moreover, morphological adaptations to local conditions contribute to plant establishment. However, the relative contributions of ploidy level and the environment to morphology have generally been neglected. Thus, the extent of morphological variation driven by ploidy level and the environment was modelled for diploid, tetraploid and hexaploid cytotypes of Campanula rotundifolia agg. Cytotype distribution was updated, and morphological and environmental differentiation was tested in the presence and absence of natural contact zones. METHODS: Cytotype distribution was assessed from 231 localities in Central Europe, including 48 localities with known chromosome counts, using flow cytometry. Differentiation in environmental niche and morphology was tested for cytotype pairs using discriminant analyses. A structural equation model was used to explore the synergies between cytotype, environment and morphology. KEY RESULTS: Tremendous discrepancies were revealed between the reported and detected cytotype distribution. Neither mixed-ploidy populations nor interploidy hybrids were detected in the contact zones. Diploids had the broadest environmental niche, while hexaploids had the smallest and specialized niche. Hexaploids and spatially isolated cytotype pairs differed morphologically, including allopatric tetraploids. While leaf and shoot morphology were influenced by environmental conditions and polyploidy, flower morphology depended exclusively on the cytotype. CONCLUSIONS: Reproductive isolation mechanisms vary between cytotypes. While diploids and polyploids are isolated postzygotically, the environmental niche shift is essential between higher polyploids. The impact of polyploidy and the environment on plant morphology implies the adaptive potential of polyploids, while the exclusive relationship between flower morphology and cytotype highlights the role of polyploidy in reproductive isolation.

The Genomic Consistency of the Loss of Anadromy in an Arctic Fish (Salvelinus alpinus).

AbstractThe potentially significant genetic consequences associated with the loss of migratory capacity of diadromous fishes that have become landlocked in freshwater are poorly understood. Consistent selective pressures associated with freshwater residency may drive repeated differentiation both between allopatric landlocked and anadromous populations and within landlocked populations (resulting in sympatric morphs). Alternatively, the strong genetic drift anticipated in isolated landlocked populations could hinder consistent adaptation, limiting genetic parallelism. Understanding the degree of genetic parallelism underlying differentiation has implications for both the predictability of evolution and management practices. We employed an 87k single-nucleotide polymorphism (SNP) array to examine the genetic characteristics of landlocked and anadromous Arctic char (Salvelinus alpinus) populations from five drainages within Labrador, Canada. One gene was detected as an outlier between sympatric, size-differentiated morphs in each of two landlocked lakes. While no single locus differentiated all replicate pairs of landlocked and anadromous populations, several SNPs, genes, and paralogs were consistently detected as outliers in at least 70% of these pairwise comparisons. A significant C-score suggested that the amount of shared outlier SNPs across all paired landlocked and anadromous populations was greater than expected by chance. Our results indicate that despite their isolation, selection due to the loss of diadromy may drive consistent genetic responses in landlocked populations.

Emission Rates of Species-Specific Volatiles Vary across Communities of Clarkia Species: Evidence for Multimodal Character Displacement.

AbstractA current frontier of character displacement research is to determine whether displacement occurs via multiple phenotypic pathways and varies across communities with different species compositions. Here, we conducted the first test for context-dependent character displacement in multimodal floral signals by analyzing variation in floral scent in a system that exhibits character displacement in flower size and that has multiple types of sympatric communities. In a greenhouse common garden experiment, we measured quantitative variation in volatile emission rates of the progeny of two species of Clarkia from replicated parental communities that contain one, two, or four Clarkia species. The first two axes of a constrained correspondence analysis, which explained 24% of the total variation in floral scent, separated the species and community types. Of the 23 compounds that were significantly correlated with these axes, nine showed patterns consistent with character displacement. Two compounds produced primarily by C. unguiculata and two compounds produced primarily by C. cylindrica were emitted in higher amounts in sympatry. Character displacement in some volatiles varied across sympatric parental communities and occurred in parallel with displacement in flower size, demonstrating that this evolutionary process can be context dependent and may occur through multiple pathways.

Hybrid breakdown is elevated near the historical cores of a species' range.

New species form when they become reproductively isolated. A classic model of speciation posits that derived mutations appear in isolated populations and reduce fitness when combined in hybrids. While these Bateson-Dobzhansky-Muller incompatibilities are known to accumulate as populations diverge over time, they may also reflect the amount of standing genetic variation within populations. We analysed the fitness of F2 hybrids in crosses between 24 populations of a plant species (Campanula americana) with broad variation in standing genetic variation and genetic differentiation driven by post-glacial range expansions. Hybrid breakdown varied substantially and was strongest between populations near the historical cores of the species range where within-population genetic diversity was high. Nearly half of the variation in hybrid breakdown was predicted by the combined effects of standing genetic variation within populations, their pairwise genetic differentiation and differences in the climates they inhabit. Hybrid breakdown was enhanced between populations inhabiting distinct climates, likely reflecting local adaptation. Results support that the mutations causing hybrid breakdown, the raw material for speciation, are more common in long-inhabited areas of the species range. Genetic diversity harboured in refugial areas is thus an important source of incompatibilities critical to the speciation process.

Asymmetric character displacement in mixed oak stands.

Ecological character displacement (ECD) refers to a pattern of increased divergence at sites where species ranges overlap caused by competition for resources. Although ECD is believed to be common, there are few in-depth studies that clearly establish its existence, especially in plants. Thus, we have compared leaf traits in allopatric and sympatric populations of two East Asian deciduous oaks: Quercus dentata and Quercus aliena. In contrast to previous studies, we define sympatry and allopatry at a local scale, thereby comparing populations that can or cannot directly interact. Using genetic markers, we found greater genetic divergence between the two oak species growing in mixed stands and inferred that long-term gene flow has predominantly occurred asymmetrically from the cold-tolerant species (Q. dentata) to the warm-demanding later colonizing species (Q. aliena). Analysis of leaf traits revealed greater divergence in mixed than in pure oak stands. This was mostly due to the later colonizing species being characterized by more resource-conservative traits in the presence of the other species. Controlling for relevant environmental differences did not alter these conclusions. These results suggest that asymmetric trait divergence can take place where species coexist, possibly due to the imbalance in demographic history of species resulting in asymmetric inter-specific selection pressures.

Genomic scale data shows that Parastacus nicoleti encompasses more than one species of burrowing continental crayfishes and that lineage divergence occurred with and without gene flow.

Delimiting species is a challenge, especially in scenarios of diversification with gene flow and when species are now allopatric where reproductive isolation cannot be directly tested. Continental burrowing crayfishes of the genus Parastacus present a disjoint distribution in southern South America. One of the species is P. nicoleti, which lives in underground waters in swampy and wooded areas of southern Chile. A previous assessment based on mitochondrial DNA sequences suggest that the taxon may represent a species complex. Here, using thousands of nuclear genomic single-nucleotide polymorphisms obtained via RADSeq from 81 specimens collected at 27 localities throughout the distributional range of the species, we apply an integrative species delimitation approach to test species boundaries and to investigate some aspects of the speciation process. Our analyses corroborate previous results; a scenario that we favor suggests that the P. nicoleti encompasses seven distinct species. Additionally, demographic analyses show that the distinct species have followed distinct trajectories in size change during the last 17.5 million years and that speciation in this group occurred both in strict isolation as well as in the presence of gene flow.

Cytonuclear discordance, reticulation and cryptic diversity in one of North America's most common frogs.

Complicated phylogenetic histories benefit from diverse sources of inference. Pseudacris crucifer (spring peeper) spans most of eastern North America and comprises six mtDNA lineages that form multiple contact zones. The putative Miocene or early Pliocene origins of the oldest lineages within Pseudacris crucifer imply sufficient time for species-level divergence. To understand why this species appears unified while congeners have radiated, we analyze and compare male advertisement calls, mitochondrial, and nuclear markers and speak to the complex processes that have potentially influenced its contemporary patterns. We find extensive geographic and topological mitonuclear discordance, with three nuclear lineages containing 6 more-structured mtDNA lineages, and nuclear introgression at some contact zones. Male advertisement call differentiation is incongruent with the genetic structure as only one lineage appears differentiated. Occupying the Interior Highlands of the central United States, this Western lineage also has the most concordant mitochondrial and nuclear geographic patterns. Based on our findings we suggest that the antiquity of common ancestors was not as important as the maintenance of allopatry in the divergence in P. crucifer genetic lineages. We use multiple lines of evidence to generate hypotheses of isolation, reticulation, and discordance within this species and to expand our understanding of the early stages of speciation.

Behavioural response to songs between genetically diverged allopatric populations of Darwin's small tree finch in the Galápagos.

Empirical data that identify contemporary mechanisms of divergence shed light on how species could multiply. In this study, we measured population genetic structure, song syllable diversity and response to simulated intruder song in Darwin's small tree finch (Camarhynchus parvulus) on Santa Cruz and Floreana Islands, Galápagos archipelago. Our aim was to test whether the magnitude of contemporary behavioural response in resident birds was consistent with patterns of genetic or cultural differences between populations. We analysed genetic structure and the occurrence of song syllable types, and experimentally measured the response of resident birds to intruder bird song from different geographical origin (i.e., island) or syllable type. We discovered a weak signal of population genetic structure between Santa Cruz and Floreana Islands. Although some song syllables occurred on both islands, others were unique to each island; Santa Cruz Island males used more unique syllables than Floreana Island males. Both Santa Cruz and Floreana resident males discriminated their response towards a simulated intruder song based on the geographical origin of the intruder song, but not on the syllable type sung by the intruder. We conclude that the populations are diverging in genetic and cultural traits and identified a signal of contemporary behavioural response that could maintain divergence upon secondary contact.

Ecological specialization and niche overlap of subterranean rodents inferred from DNA metabarcoding diet analysis.

Knowledge of how animal species use food resources available in the environment can increase our understanding of many ecological processes. However, obtaining this information using traditional methods is difficult for species feeding on a large variety of food items in highly diverse environments. We amplified the DNA of plants for 306 scat and 40 soil samples, and applied an environmental DNA metabarcoding approach to investigate food preferences, degree of diet specialization and diet overlap of seven herbivore rodent species of the genus Ctenomys distributed in southern and midwestern Brazil. The metabarcoding approach revealed that these species consume more than 60% of the plant families recovered in soil samples, indicating generalist feeding habits of ctenomyids. The family Poaceae was the most common food resource retrieved in scats of all species as well in soil samples. Niche overlap analysis indicated high overlap in the plant families and molecular operational taxonomic units consumed, mainly among the southern species. Interspecific differences in diet composition were influenced, among other factors, by the availability of resources in the environment. In addition, our results provide support for the hypothesis that the allopatric distributions of ctenomyids allow them to exploit the same range of resources when available, possibly because of the absence of interspecific competition.

Changing Ecological Opportunities Facilitated the Explosive Diversification of New Caledonian Oxera (Lamiaceae).

Phylogenies recurrently demonstrate that oceanic island systems have been home to rapid clade diversification and adaptive radiations. The existence of adaptive radiations posits a central role of natural selection causing ecological divergence and speciation, and some plant radiations have been highlighted as paradigmatic examples of such radiations. However, neutral processes may also drive speciation during clade radiations, with ecological divergence occurring following speciation. Here, we document an exceptionally rapid and unique radiation of Lamiaceae within the New Caledonian biodiversity hotspot. Specifically, we investigated various biological, ecological, and geographical drivers of species diversification within the genus Oxera. We found that Oxera underwent an initial process of rapid cladogenesis likely triggered by a dramatic period of aridity during the early Pliocene. This early diversification of Oxera was associated with an important phase of ecological diversification triggered by significant shifts of pollination syndromes, dispersal modes, and life forms. Finally, recent diversification of Oxera appears to have been further driven by the interplay of allopatry and habitat shifts likely related to climatic oscillations. This suggests that Oxera could be regarded as an adaptive radiation at an early evolutionary stage that has been obscured by more recent joint habitat diversification and neutral geographical processes. Diversification within Oxera has perhaps been triggered by varied ecological and biological drivers acting in a leapfrog pattern, but geographic processes may have been an equally important driver. We suspect that strictly adaptive radiations may be rare in plants and that most events of rapid clade diversification may have involved a mixture of geographical and ecological divergence.

Geography of speciation affects rate of trait divergence in haemulid fishes.

Speciation and the interactions between recently diverged species are thought to be major causes of ecological and morphological divergence in evolutionary radiations. Here, we explore the extent to which geographical overlap and time since speciation may promote divergence in marine species, which represent a small fraction of currently published studies about the patterns and processes of speciation. A time-calibrated molecular phylogeny of New World haemulid fishes, a major radiation of reef and shore fishes in the tropical West Atlantic and East Pacific, reveals 21 sister species pairs, of which eight are fully sympatric and 13 are allopatric. Sister species comparisons show a non-significant relation between most of the phenotypic traits and time since divergence in allopatric taxa. Additionally, we find no difference between sympatric and allopatric pairs in the rate of divergence in colour pattern, overall body shape, or functional morphological traits associated with locomotion or feeding. However, sympatric pairs show a significant decrease in the rate of divergence in all of these traits with increasing time since their divergence, suggesting an elevated rate of divergence at the time of speciation, the effect of which attenuates as divergence time increases. Our results are consistent with an important role for geographical overlap driving phenotypic divergence early in the speciation process, but the lack of difference in rates between sympatric and allopatric pairs indicates that the interactions between closely related species are not dominant drivers of this divergence.

Current geography masks dynamic history of gene flow during speciation in northern Australian birds.

Genome divergence is greatly influenced by gene flow during early stages of speciation. As populations differentiate, geographic barriers can constrain gene flow and so affect the dynamics of divergence and speciation. Current geography, specifically disjunction and continuity of ranges, is often used to predict the historical gene flow during the divergence process. We test this prediction in eight meliphagoid bird species complexes codistributed in four regions. These regions are separated by known biogeographical barriers across northern Australia and Papua New Guinea. We find that bird populations currently separated by terrestrial habitat barriers within Australia and marine barriers between Australia and Papua New Guinea have a range of divergence levels and probability of gene flow not associated with current range connectivity. Instead, geographic distance and historical range connectivity better predict divergence and probability of gene flow. In this dynamic environmental context, we also find support for a nonlinear decrease of the probability of gene flow during the divergence process. The probability of gene flow initially decreases gradually after a certain level of divergence is reached. Its decrease then accelerates until the probability is close to zero. This implies that although geographic connectivity may have more of an effect early in speciation, other factors associated with higher divergence may play a more important role in influencing gene flow midway through and later in speciation. Current geographic connectivity may then mislead inferences regarding potential for gene flow during speciation under a complex and dynamic history of geographic and reproductive isolation.

Biogeography of Mesalina (Reptilia: Lacertidae), with special emphasis on the Mesalina adramitana group from Arabia and the Socotra Archipelago.

The lacertid lizards of the genus Mesalina inhabit the arid regions of the Old World, from North Africa to NW India. Of the 19 recognized species within the genus, eleven occur in Arabia. In this study, we explore the genetic variability and phylogeographic patterns of the less studied M. adramitana group from southern Arabia and the Socotra Archipelago within the phylogenetic and biogeographic context of the entire genus. Our unprecedented sampling extends the distribution ranges of most Mesalina species and, for the first time, sequences of M. ayunensis are included in a phylogenetic analysis. We perform analyses of concatenated multilocus datasets and species trees, conduct species delimitation analyses, and estimate divergence times within a biogeographic framework. Additionally, we inferred the environmental suitability and identified dispersal corridors through which gene flow is enabled within M. adramitana. Our results show that the Socotra Archipelago was colonized approximately 7 Mya by a single oversea colonization from mainland Arabia. Then, an intra-archipelago dispersal event that occurred approximately 5 Mya resulted in the speciation between M. balfouri, endemic to Socotra, Samha and Darsa Islands, and M. kuri, endemic to Abd al Kuri Island. Similar to previous studies, we uncovered high levels of genetic diversity within the M. adramitana species-group, with two highly divergent lineages of M. adramitana living in allopatry and adapted to locally specific climatic conditions that necessitate further investigation.

Speciation Post Synthesis: 1960-2000.

Speciation-the origin of new species-has been one of the most active areas of research in evolutionary biology, both during, and since the Modern Synthesis. While the Modern Synthesis certainly shaped research on speciation in significant ways, providing a core framework, and set of categories and methods to work with, the history of work on speciation since the mid-twentieth century is a history of divergence and diversification. This piece traces this divergence, through both theoretical advances, and empirical insights into how different lineages, with different genetics and ecological conditions, are shaped by very different modes of diversification.

Synchronous diversification of parachuting frogs (Genus Rhacophorus) on Sumatra and Java.

Geological and climatological processes can drive the synchronous diversification of co-distributed species. The islands of Sumatra and Java have experienced complex geological and climatological histories, including extensive sea-level changes and the formation of valleys between northern, central, and southern components of the Barisan Mountain Range, which may have promoted diversification of their resident species. We investigate diversification on these islands using 13 species of the parachuting frog genus Rhacophorus. We use both mitochondrial and nuclear sequence data, along with genome-wide SNPs to estimate phylogenetic structure and divergence times, and to test for synchronous diversification. We find support for synchronous divergence among sister-species pairs from Sumatra and Java ∼9 Ma, as well as of populations of four co-distributed taxa on Sumatra ∼5.6 Ma. We found that sister species diverged in allopatry on Sumatra and conclude that divergence on Sumatra and Java was affected by sea-level fluctuations that promoted isolation in allopatry.

Ecological sorting and character displacement contribute to the structure of communities of Clarkia species.

Despite long-standing interest in the evolutionary ecology of plants that share pollinators, few studies have explored how these interactions may affect communities during both community assembly (ecological sorting) and through ongoing, in situ evolution (character displacement), and how the effects of these interactions may change with community context. To determine if communities display patterns consistent with ecological sorting, we assessed the frequency of co-occurrence of four species of Clarkia in the southern Sierra foothills (Kern County, CA, USA). To investigate potential character displacement, we measured pollination-related traits on plants grown in a greenhouse common garden from seed collected in communities with one, two or four Clarkia species. Among the four species of Clarkia in this region, the two species that are often found in multi-species communities also co-occur with one another more frequently than expected under a null model. This pattern is consistent with ecological sorting, although further investigation is needed to determine the role of pollinators in shaping community assembly. Patterns of trait variation in a common garden suggest that these two species have diverged in floral traits and converged in flowering time where they co-occur, which is consistent with character displacement. Trait variation across community types also suggests that the process and outcome of character displacement may vary with community context. Because community context appears to affect both the direction and magnitude of character displacement, change in more species-rich communities may not be predictable from patterns of change in simpler communities.