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Data from: Behavioural mechanisms of sexual isolation involving multiple modalities and their inheritance

Speciation research dissects the genetics and evolution of reproductive barriers between parental species. Hybrids are the 'gatekeepers' of gene flow, so it is also important to understand the behavioural mechanisms and genetics of any potential isolation from their parental species. We tested the role of multiple behavioural barriers in reproductive isolation among closely related field crickets and their hybrids (Teleogryllus oceanicus and T. commodus). These species hybridise in the laboratory, but the behaviour of hybrids is unusual and there is little evidence for gene flow in the wild. We found that heterospecific pairs exhibited reduced rates of courtship behaviour due to discrimination by both sexes, and that this behavioural isolation was symmetrical. However, hybrids were not sexually selected against and exhibited high rates of courtship behaviour even though hybrid females are sterile. Using reciprocal hybrid crosses, we characterized patterns of interspecific divergence and inheritance in key sexual traits that might underlie the mating patterns we found: calling song, courtship song and cuticular hydrocarbons (CHCs). Song traits exhibited both sex-linkage and transgressive segregation, whereas CHCs exhibited only the latter. Calculations of the strength of isolation exerted by these sexual traits suggest that close-range signals are as important as long-distance signals in contributing to interspecific sexual isolation. The surprisingly weak mating barriers observed between hybrids and parental species highlights the need to examine reproductive isolating mechanisms and their genetic bases across different potential stages of introgressive hybridisation.

Data from: Reproductive isolation in a nascent species pair is associated with aneuploidy in hybrid offspring

Speciation may occur when the genomes of two populations accumulate genetic incompatibilities and/or chromosomal rearrangements that prevent inter-breeding in nature. Chromosome stability is critical for survival and faithful transmission of the genome, and hybridization can compromise this. However, the role of chromosomal stability on hybrid incompatibilities has rarely been tested in recently diverged populations. Here, we test for chromosomal instability in hybrids between nascent species, the 'dwarf' and 'normal' lake whitefish (Coregonus clupeaformis). We examined chromosomes in pure embryos, and healthy and malformed backcross embryos. While pure individuals displayed chromosome numbers corresponding to the expected diploid number (2n = 80), healthy backcrosses showed evidence of mitotic instability through an increased variance of chromosome numbers within an individual. In malformed backcrosses, extensive aneuploidy corresponding to multiples of the haploid number (1n = 40, 2n = 80, 3n = 120) was found, suggesting meiotic breakdown in their F1 parent. However, no detectable chromosome rearrangements between parental forms were identified. Genomic instability through aneuploidy thus appears to contribute to reproductive isolation between dwarf and normal lake whitefish, despite their very recent divergence (approx. 15–20 000 generations). Our data suggest that genetic incompatibilities may accumulate early during speciation and limit hybridization between nascent species.

Data from: A practical introduction to microbial molecular ecology through the use of isolation chips

In the context of anti-microbial resistance as one of the most serious issues faced globally by health providers, we explored a practical introduction to molecular microbial ecology. We designed field work and practical experiments for third year members of a four year undergraduate Masters Programme in which the students employed traditional and novel isolation techniques to identify antimicrobial activities from soil dwelling microorganisms. Students gained experience in isolating DNA from complex microbial communities, amplifying 16S rRNA genes and applied richness / diversity indices as well as principal coordinates analyses to the interpretation of the data they obtained from high throughput sequencing. Our results confirmed that isolation chips (iChips) facilitate the growth of a greater diversity and different species subset from the complex soil microorganism community than traditional plate spreading techniques. However, rarefaction of 16S rRNA amplicon sequencing data showed that the majority of observed species in soil remain unculturable by current methods. Based on the written reports produced by the students carrying out the work, we concluded that the described protocols are robust and informative, that these activities provide a good practical introduction to the theories and practice of molecular ecology and can be easily deployed to groups of six or more students in a cost-effective manner.

opencc-zeroDec 2011View details →

Data from: A test for environmental effects on behavioral isolation in two species of killifish

Behavioral isolation is a common and potent mechanism of reproductive isolation. Determining the extent to which behavioral isolation varies with environmental conditions is critical to understanding speciation and the maintenance of species boundaries. Here, we tested the effect of salinity on behavioral isolation (female species recognition, male-male competition, male species recognition) between two closely related killifish (Lucania goodei and L. parva) that differ in salinity tolerance. We performed no-choice assays and behavioral trials where males could compete and court females in fresh water (0 ppt) and brackish water (15 ppt). We found high levels of behavioral isolation that did not vary as a function of salinity. In behavioral trials, male species recognition of females was strong and asymmetric between the two species. Lucania goodei males preferred conspecifics and rarely courted or mated with L. parva females. Lucania parva males preferred conspecifics but readily courted and mated with L. goodei females. This asymmetry matches previously documented asymmetries in hybrid offspring fitness. Crosses between L. parva males and L. goodei females produce fully viable/fertile hybrids, but crosses between L. goodei males and L. parva females produce males with reduced fertility. Hence, behavioral isolation may have evolved in part due to reinforcement.

Data from: A unique ecological niche fosters hybridization of oak-tree and vineyard isolates of Saccharomyces cerevisiae.

Differential adaptation to distinct niches can restrict gene flow and promote population differentiation within a species. However, in some cases the distinction between niches can collapse, forming a hybrid niche with features of both environments. We previously reported that distinctions between vineyards and oak soil present an ecological barrier that restricts gene flow between lineages of Saccharomyces cerevisiae. Vineyard isolates are tolerant to stresses associated with grapes while North American oak strains are particularly tolerant to freeze-thaw cycles. Here, we report the isolation of Saccharomyces cerevisiae strains from Wisconsin cherry trees, which display features common to vineyards (e.g. high sugar concentrations) and frequent freeze-thaw cycles. Genome sequencing revealed that the isolated strains are highly heterozygous and represent recent hybrids of the oak x vineyard lineages. We found that the hybrid strains are phenotypically similar to vineyard strains for some traits, but are more similar to oak strains for other traits. The cherry strains were exceptionally good at growing in cherry juice, raising the possibility that they have adapted to this niche. We performed transcriptome profiling in cherry, oak, and vineyard strains and show that the cherry-tree hybrids display vineyard-like or oak-like expression, depending on the gene sets, and in some cases the expression patterns linked back to shared stress tolerances. Allele-specific expression in these natural hybrids suggested concerted cis-regulatory evolution at sets of functionally regulated genes. Our results raise the possibility that hybridization of the two lineages provides a genetic solution to the thriving in this unique niche.

opencc-zeroDec 2012View details →

Data from: Strength and variability of postmating reproductive isolating barriers between four European white oak species

The identification and quantification of the relative importance of reproductive isolating barriers is of fundamental importance to understand species maintenance in the face of interspecific gene flow between hybridizing species. Yet, such assessments require extensive experimental fertilisations that are particularly difficult when dealing with more than two hybridizing and long generation time species such as oaks. Here we quantify the relative contribution of four postmating reproductive isolating barriers consisting of two prezygotic barriers (gametic incompatibility, conspecific pollen precedence) and two postzygotic barriers (germination rate, early survival) from extensive controlled pollinations between four oak species (Quercus robur, Q. petraea, Q. pubescens and Q. pyrenaica) that have been shown to frequently hybridize in natural populations. We found high variation in the strength of total reproductive isolation between species, ranging from total reproductive isolation to advantage toward hybrid formation. As previously found, Q. robur pollen was unable to fertilize Q. petraea due to a strong reproductive isolating mechanism. On the contrary, Q. pubescens pollen was more efficient at fertilizing Q. petraea than conspecific pollen. Overall, prezygotic barriers contribute far more than postzygotic barriers to isolate species reproductively, suggesting a role for reinforcement in the development of prezygotic barriers. Conspecific pollen precedence reduced hybrid formation when pollen competition was allowed, however presence of conspecific pollen did not totally prevent hybridization. Our results suggest that pollen competition depends on multiple ecological and environmental parameters, including species local abundance, and that it may be of uppermost importance to understand interspecific gene flow among natural multispecies populations.

Data from: The relationship between post-mating reproductive isolation and reinforcement in Phlox

The process of speciation involves the accumulation of reproductive isolation (RI) between diverging lineages. Selection can favor increased RI via the process of reinforcement, whereby costs to hybridization impose selection for increased prezygotic RI. Reinforcement results in phenotypic divergence within at least one taxon, as a result of costly hybridization between sympatric taxa. The strength of selection driving reinforcement is determined by the cost of hybridization and the frequency of hybridization. We investigated the cost of hybridization by quantifying post-mating RI barriers among Phlox species that comprise one of the best-studied cases of reinforcement. We determined if the strength of RI differs among lineages that have and have not undergone reinforcement, how much variability there is within species in RI, and whether RI is associated with phylogenetic relatedness. We found high RI for the species that underwent phenotypic divergence due to reinforcement; however, RI was also high between other species pairs. We found extensive variability in RI among individuals within species, and no evidence that the strength of RI was associated with phylogenetic relatedness. We suggest that phenotypic divergence due to reinforcement is associated with the frequency of hybridization and introgression, and not the cost of hybridization in this clade.

Data from: Patterns of reproductive isolation in a haplodiploid – strong post‐mating, prezygotic barriers among three forms of a social spider mite

In speciation research, much attention is paid to the evolution of reproductive barriers, preventing diverging groups from hybridizing back into one gene pool. The prevalent view is that reproductive barriers evolve gradually as a byproduct of genetic changes accumulated by natural selection and genetic drift in groups that are segregated spatially and/or temporally. Reproductive barriers, however, can also be reinforced by natural selection against maladaptive hybridization. These mutually compatible theories are both empirically supported by studies, analyzing relationships between intensity of reproductive isolation and genetic distance in sympatric taxa and allopatric taxa. Here, we present the – to our knowledge – first comparative study in a haplodiploid organism, the social spider mite Stigmaeopsis miscanthi, by measuring premating and postmating pre- and postzygotic components of reproductive isolation, using three recently diverged forms of the mite that partly overlap in home range. We carried out cross experiments and measured genetic distances (mtDNA and nDNA) among parapatric and allopatric populations of the three forms. Our results show that the three forms are reproductively isolated, despite the absence of premating barriers, and that the postmating, prezygotic component contributes most to reproductive isolation. As expected, the strength of postmating reproductive barriers positively correlated with genetic distance. We did not find a clear pattern of prezygotic barriers evolving faster in parapatry than in allopatry, although one form did show a trend in line with the ecological and behavioral relationships between the forms. Our study advocates the versatility of haplodiploid animals for investigating the evolution of reproductive barriers.

opencc-zeroDec 2015View details →

Data from: Assessing reproductive isolation using a contact zone between parapatric lake-stream stickleback ecotypes

Ecological speciation occurs when populations evolve reproductive isolation as a result of divergent natural selection. This isolation can be influenced by many potential reproductive barriers, including selection against hybrids, selection against migrants, and assortative mating. How and when these barriers act and interact in nature is understood for relatively few empirical systems. We used a mark-recapture experiment in a contact zone between lake and stream three-spined sticklebacks (Gasterosteus aculeatus, Linnaeus) to evaluate the occurrence of hybrids (allowing inferences about reproductive isolation), the inter-annual survival of hybrids (allowing inferences about selection against hybrids), and the shift in lake-like versus stream-like characteristics (allowing inferences about selection against migrants). Genetic and morphological data suggest the occurrence of hybrids and no selection against hybrids in general, a result contradictory to a number of other studies of sticklebacks. However, we did find selection against more lake-like individuals, suggesting a barrier to gene flow from the lake into the stream. Combined with previous work on this system, our results suggest that multiple (most weakly and often asymmetric) barriers must be combining to yield substantial restrictions on gene flow. This work provides evidence of a reproductive barrier in lake-stream sticklebacks and highlights the value of assessing multiple reproductive barriers in natural contexts.

Data from: Reproductive isolation with a learned trait in a structured population

Assortative mating displays and/or preferences can be affected by learning across a wide range of animal taxa, but the specifics of how this learning affects speciation with gene flow are not well understood. We use population genetic models with trait learning to investigate how the identity of the tutor affects the divergence of a self-referent phenotype-matching trait. We find that oblique learning (learning from unrelated individual of the previous generation) and maternal learning mask sexual selection and therefore do not allow the maintenance of divergence. In contrast, by enhancing positive frequency-dependent sexual selection, paternal learning can maintain more divergence than genetic inheritance, but leads to the loss of polymorphism more easily. Furthermore, paternal learning inhibits the invasion of a novel self-referent phenotype-matching trait, especially in a large population.

opencc-zeroDec 2016View details →

Data from: Measuring CO2 and HCO3- permeabilities of isolated chloroplasts using a MIMS-18O approach

To support photosynthetic CO2 fixation by Rubisco, the chloroplast must be fed with inorganic carbon in the form of CO2 or bicarbonate. However, the mechanisms allowing the rapid passage of this gas and this charged molecule through the bounding membranes of the chloroplast envelope are not yet completely elucidated. We describe here a method allowing us to measure the permeability of these two molecules through the chloroplast envelope using a membrane inlet mass spectrometer and 18O-labelled inorganic carbon. We established that the internal stromal carbonic anhydrase activity is not limiting for this technique, and precisely measured the chloroplast surface area and permeability values for CO2 and bicarbonate. This was performed on chloroplasts from several plant species, with values ranging from 2.3 × 10–4 m s–1 to 8 × 10–4 m s–1 permeability for CO2 and 1 × 10–8 m s–1 for bicarbonate. We were able to apply our method to chloroplasts from an Arabidopsis aquaporin mutant, and this showed that CO2 permeability was reduced 50% in the mutant compared with the wild-type reference.

Data from: Resource stability and geographic isolation are associated with genome divergence in western Palearctic crossbills

While many conifers produce annually variable seed crops, serotinous species (which hold seeds in cones for multiple years) represent unusually stable food resources for seed predators. Such stability is conducive to residency and potentially population divergence of consumers as exemplified by the Cassia crossbill (Loxia sinesciuris) in North America. We used genotyping-by-sequencing to test whether three Mediterranean subspecies of common crossbills (L. curvirostra) associated with the serotinous Aleppo pine (Pinus halepensis) were more genetically distinct than European crossbills associated with non-serotinous conifers. We assembled a Cassia crossbill draft genome as a reference for mapping GBS reads, and as a first step towards a more contiguous genome assembly. We found clear patterns of genetic divergence for each of the P. halepensis-associated subspecies. Geographic isolation, as promoted by resource stability and residency, is associated with genetic divergence of two of these subspecies. However, geographic isolation cannot account for divergence of L. c. hispana. Instead, resource stability likely contributed to divergence by reducing dispersal and increasing resource competition that may limit breeding by immigrants. In contrast, we found no differentiation among common crossbills associated with less stable resources, and only slight differentiation between common crossbills and parrot crossbills (L. pytyopsittacus). The substantial morphological divergence between common and parrot crossbills has likely originated or been maintained by selection despite gene flow generated by spatiotemporal resource fluctuation. Our results indicate that phenological as well as morphological characteristics of conifers have influenced crossbill diversification, and suggest a possible link between resource stability and population divergence.

opencc-zeroOct 2019View details →

Data from: Biotransformation of chlorothalonil by strain Stenotrophomonas acidaminiphila BJ1 isolated from farmland soil

The chlorothalonil is a widely used fungicide while the contamination of soil and water environments by this chemical causes potential threats to the biodiversity. Given the metabolic potential of soil microorganisms, there is a need for developing microbiological approaches to degrade persistent compounds, such as chlorothalonil, in the contaminated sites. Here in this study, we isolated a bacterial strain (namely, BJ1) capable of degrading chlorothalonil from a chlorothalonil-contaminated farmland soil in the Shandong Province, China. Using 16S rDNA gene sequencing, morphological and biological characteristics, we identified the strain BJ1 as Stenotrophomonas acidaminiphila. The strain BJ1 utilizes chlorothalonil as a sole carbon source. At initial concentrations of 50, 100, 200, 300 mg l-1, it degraded 91.5%, 89.4%, 86.5 and 83.5% of chlorothalonil after 96 h of inoculation under optimum conditions (30 °C and pH 7.0), respectively. Two metabolites, methyl-2, 5, 6-trichloro-3-cyano-4-methoxy-benzoate and methyl-3- cyano-2, 4, 5, 6-tetrachlorobenzoate, were detected and identified based on HPLC-MS analysis, which suggests that the strain BJ1 metabolized chlorothalonil through the hydroxylation of chloro-group and hydration of cyano-group. The results of this study highlight the great potential for this bacterium to be used in chlorothalonil pollution remediation.

Data from: Hybridization in the Drosophila melanogaster subgroup: incomplete isolation among the three species of the yakuba complex

In the Drosophila melanogaster subgroup, the yakuba species complex, D. yakuba, D. santomea and D. teissieri have identical mitochondrial genomes in spite of nuclear differentiation. The first two species can be readily hybridized in the laboratory, and produce fertile females and sterile males. They also form hybrids in natural conditions. Nonetheless, the third species, D. teissieri, was thought to be unable to produce hybrids with either D. yakuba or D. santomea. This in turn posed the conundrum of why the three species shared a single mitochondrial genome. In this report we show that D. teissieri can indeed hybridize with both D. yakuba and D. santomea. The resulting female hybrids from both crosses are fertile, while the hybrid males are sterile. We also characterize six isolating mechanisms that might be involved in keeping the three species apart. Our results open the possibility of studying the history of introgression in the yakuba species complex and dissecting the genetic basis of interspecific differences between these three species by genetic mapping.

opencc-zeroDec 2012View details →

Data from: Genetic architecture of isolation between two species of Silene with sex chromosomes and Haldane's rule

Examination of the genetic architecture of hybrid breakdown can provide insight into the genetic mechanisms of commonly observed isolating phenomena such as Haldane's rule. We used line-cross analysis to dissect the genetic architecture of divergence between two plant species that exhibit Haldane's rule for male sterility and rarity, Silene latifolia and Silene diclinis. We made 15 types of crosses, including reciprocal F1, F2, backcrosses, and later-generation crosses, grew the seeds to flowering, and measured the number of viable ovules, proportion of viable pollen, and sex ratio. Typically, Haldane's rule for male rarity in XY animal hybrids is explained by interactions involving recessive X-linked alleles that are deleterious when hemizygous (dominance theory), while sterility is explained by rapid evolution of spermatogenesis genes (faster-male evolution). In contrast, we found that the genetic mechanisms underlying Haldane's rule between the two Silene species did not follow these conventions. Dominance theory was sufficient to explain male sterility, but male rarity likely involved faster-male evolution. We also found an effect of the neo-sex chromosomes of S. diclinis on the extreme rarity of some hybrid males. Our findings suggest that the genetic architecture of Haldane's rule in dioecious plants may differ from those commonly found in animals.

Data from: Isolation by resistance across a complex coral reef seascape

A detailed understanding of the genetic structure of populations and an accurate interpretation of processes driving contemporary patterns of gene flow are fundamental to successful spatial conservation management. The field of seascape genetics seeks to incorporate environmental variables and processes into analyses of population genetic data to improve our understanding of forces driving genetic divergence in the marine environment. Information about barriers to gene flow (such as ocean currents) is used to define a resistance surface to predict the spatial genetic structure of populations and explain deviations from the widely applied isolation-by-distance model. The majority of seascape approaches to date have been applied to linear coastal systems or at large spatial scales (more than 250 km), with very few applied to complex systems at regional spatial scales (less than 100 km). Here, we apply a seascape genetics approach to a peripheral population of the broadcast-spawning coral Acropora spicifera across the Houtman Abrolhos Islands, a high-latitude complex coral reef system off the central coast of Western Australia. We coupled population genetic data from a panel of microsatellite DNA markers with a biophysical dispersal model to test whether oceanographic processes could explain patterns of genetic divergence. We identified significant variation in allele frequencies over distances of less than 10 km, with significant differentiation occurring between adjacent sites but not between the most geographically distant ones. Recruitment probabilities between sites based on simulated larval dispersal were projected into a measure of resistance to connectivity that was significantly correlated with patterns of genetic divergence, demonstrating that patterns of spatial genetic structure are a function of restrictions to gene flow imposed by oceanographic currents. This study advances our understanding of the role of larval dispersal on the fine-scale genetic structure of coral populations across a complex island system and applies a methodological framework that can be tailored to suit a variety of marine organisms with a range of life-history characteristics.

opencc-zeroDec 2015View details →

Data from: Competition-driven build-up of habitat isolation and selection favouring dispersal modification in a young avian hybrid zone

Competition-driven evolution of habitat isolation is an important mechanism of ecological speciation but empirical support for this process is often indirect. We examined how an on-going displacement of pied flycatchers from their preferred breeding habitat by collared flycatchers in a young secondary contact zone is associated with (a) access to an important food resource (caterpillar larvae), (b) immigration of pied flycatchers in relation to habitat quality, and (c) the risk of hybridization in relation to habitat quality. Over the past 12 years, the estimated access to caterpillar larvae biomass in the habitat surrounding the nests of pied flycatchers has decreased by a fifth due to shifted establishment possibilities, especially for immigrants. However, breeding in the high quality habitat has become associated with such a high risk of hybridization for pied flycatchers that overall selection currently favors pied flycatchers that were forced to immigrate into the poorer habitats (despite lower access to preferred food items). Our results show that competition-driven habitat segregation can lead to fast habitat isolation, which per se caused an opportunity for selection to act in favor of future "voluntarily" altered immigration patterns and possibly strengthened habitat isolation through reinforcement.

opencc-zeroDec 2012View details →

Data from: Population size and time since island isolation determine genetic diversity loss in insular frog populations

Understanding the factors that contribute to loss of genetic diversity in fragmented populations is crucial for conservation measurements. Land-bridge archipelagoes offer ideal model systems for identifying the long-term effects of these factors on genetic variations in wild populations. In this study, we used 9 microsatellite markers to quantify genetic diversity and differentiation of 810 pond frogs (Pelophylax nigromaculataus) from 24 islands of the Zhoushan Archipelago and 3 sites on nearby mainland China and estimated the effects of the island area, population size, time since island isolation, distance to the mainland and distance to the nearest larger island on reduced genetic diversity of insular populations. The mainland populations displayed higher genetic diversity than insular populations. Genetic differentiations and no obvious gene flow were detected among the frog populations on the islands. Hierarchical partitioning analysis showed that only time since island isolation (square root transformed) and population size (log transformed) significantly contributed to insular genetic diversity. These results suggest that decreased genetic diversity and genetic differentiations among insular populations may have been caused by random genetic drift following isolation by rising sea levels during the Holocene. The results provide strong evidence for a relationship between retained genetic diversity and population size and time since island isolation for pond frogs on the islands, consistent with the prediction of the neutral theory for finite populations. Our study highlights the importance of the size and estimated isolation time of populations in understanding the mechanisms of genetic diversity loss and differentiation in fragmented wild populations.

opencc-zeroDec 2016View details →

Data from: The rate of evolution of postmating-prezygotic reproductive isolation in Drosophila

Reproductive isolation (RI) is an intrinsic aspect of species, as described in the Biological Species Concept. For that reason, the identification of the precise traits and mechanisms of RI, and the rates at which they evolve, is crucial to understanding how species originate and persist. Nonetheless, precise measurements of the magnitude of reproductive isolation are rare. Previous work has measured the rates of evolution of prezygotic and postzygotic barriers to gene flow, yet no systematic analysis has carried out the study of the rates of evolution of postmating-prezygotic (PMPZ) barriers. We systematically measured the magnitude of two barriers to gene flow that act after mating occurs but before zygotic fertilization and also measured a premating (female mating rate in nonchoice experiments) and two postzygotic barriers (hybrid inviability and hybrid sterility) for all pairwise crosses of species within the Drosophila melanogaster subgroup. Our results indicate that PMPZ isolation evolves faster than hybrid inviability but slower than premating isolation. We also describe seven new interspecific hybrids in the group. Our findings open up a large repertoire of tools that will enable researchers to manipulate hybrids and explore the genetic basis of interspecific differentiation, reproductive isolation, and speciation.