Limited effective gene flow between two interfertile red oak species

Key message

Highly elevated differentiation in different life stages between two interfertile oak species at a CONSTANS -like gene suggests a role of this gene in pre-zygotic isolation and adaptive divergence between species.

Abstract

Genome-wide differentiation patterns among oak species suggest that divergent selection can maintain species-specific adaptations and morphological integrity by reducing effective interspecific gene flow. While there is evidence for both pre- and post-zygotic isolation mechanisms in oaks (e.g., differences in flowering time, selection against hybrids), these mechanisms are rarely studied at each life stage from acorns to adult trees within the same forest. To assess the reproductive isolation mechanisms between two ecologically divergent species, we (1) quantified the number of hybrids in different life stages in Quercus rubra and Quercus ellipsoidalis, two interfertile red oaks with different adaptations to drought, and (2) assessed the timing of bud burst in both natural populations and in a seedling common garden trial. The low number of hybrids in all life stages suggested pre-zygotic isolation between species or selection in very early life stages that have not been sampled (e.g., early seed abortion). Significant differences in bud burst were found in two consecutive years between species in a common garden seedling trial but not in natural populations of the same provenance. In addition, we found evidence for divergent selection on several gene loci between species in each life stage. In particular, an SSR repeat located within the coding sequence of a CONSTANS-like gene, a locus involved in the photoperiodic regulation of flowering time and development, showed very high interspecific differentiation between species in all life stages (mean F _ST = 0.83), compared to the average neutral differentiation of 3.7 %.

     

Invasion facilitates hybridization with introgression in the Rattus rattus species complex

Biological invasions result in novel species interactions, which can have significant evolutionary impacts on both native and invading taxa. One evolutionary concern with invasions is hybridization among lineages that were previously isolated, but make secondary contact in their invaded range(s). Black rats, consisting of several morphologically very similar but genetically distinct taxa that collectively have invaded six continents, are arguably the most successful mammalian invaders on the planet. We used mitochondrial cytochrome b sequences, two nuclear gene sequences (Atp5a1 and DHFR) and nine microsatellite loci to examine the distribution of three invasive black rat lineages (Rattus tanezumi, Rattus rattus I and R. rattus IV) in the United States and Asia and to determine the extent of hybridization among these taxa. Our analyses revealed two mitochondrial lineages that have spread to multiple continents, including a previously undiscovered population of R. tanezumi in the south‐eastern United States, whereas the third lineage (R. rattus IV) appears to be confined to Southeast Asia. Analyses of nuclear DNA (both sequences and microsatellites) suggested significant hybridization is occurring among R. tanezumi and R. rattus I in the United States and also suggest hybridization between R. tanezumi and R. rattus IV in Asia, although further sampling of the latter species pair in Asia is required. Furthermore, microsatellite analyses suggest unidirectional introgression from both R. rattus I and R. rattus IV into R. tanezumi. Within the United States, introgression appears to be occurring to such a pronounced extent that we were unable to detect any nuclear genetic signal for R. tanezumi, and a similar pattern was detected in Asia.     

Evidence for gene flow in parasitic nematodes between two host species of shrews

We describe the genetic structure of populations of the intestinal nematode Longistriata caudabullata (Trichostrongyloidea: Heligmosomidae), a common parasite of short-tailed shrews (genus Blarina, Insectivora: Soricidae). Parasites and hosts were collected from a transect across a contact zone between two species of hosts, Blarina brevicauda and B. hylophaga, in central North America. An 800-base pairs (bp) fragment of the ND4 mitochondrial DNA (mtDNA) gene was sequenced for 28 worms and a 783-bp fragment of the mtDNA control region was analysed for 16 shrews. Phylogenetic analyses of mtDNA sequences revealed reciprocal monophyly for the shrew species, concordant with morphological diagnosis, and supported the idea that the transect cuts through a secondary contact zone between well-differentiated B. brevicauda and B. hylophaga. In contrast to this pattern, the parasitic nematode mtDNA phylogeny was not subdivided according to host affiliation. Genealogical discordance between parasite and host phylogenies suggests extensive gene flow among parasites across the host species boundary.     

Widespread gene flow between oceans in a pelagic seabird species complex

Global‐scale gene flow is an important concern in conservation biology as it has the potential to either increase or decrease genetic diversity in species and populations. Although many studies focus on the gene flow between different populations of a single species, the potential for gene flow and introgression between species is understudied, particularly in seabirds. The only well‐studied example of a mixed‐species, hybridizing population of petrels exists on Round Island, in the Indian Ocean. Previous research assumed that Round Island represents a point of secondary contact between Atlantic (Pterodroma arminjoniana) and Pacific species (Pterodroma neglecta and Pterodroma heraldica). This study uses microsatellite genotyping and tracking data to address the possibility of between‐species hybridization occurring outside the Indian Ocean. Dispersal and gene flow spanning three oceans were demonstrated between the species in this complex. Analysis of migration rates estimated using bayesass revealed unidirectional movement of petrels from the Atlantic and Pacific into the Indian Ocean. Conversely, structure analysis revealed gene flow between species of the Atlantic and Pacific oceans, with potential three‐way hybrids occurring outside the Indian Ocean. Additionally, geolocation tracking of Round Island petrels revealed two individuals travelling to the Atlantic and Pacific. These results suggest that interspecific hybrids in Pterodroma petrels are more common than was previously assumed. This study is the first of its kind to investigate gene flow between populations of closely related Procellariiform species on a global scale, demonstrating the need for consideration of widespread migration and hybridization in the conservation of threatened seabirds.     

Hybrid zones and the genetic architecture of a barrier to gene flow between two sunflower species.

Genetic analyses of reproductive barriers represent one of the few methods by which theories of speciation can be tested. However, genetic study is often restricted to model organisms that have short generation times and are easily propagated in the laboratory. Replicate hybrid zones with a diversity of recombinant genotypes of varying age offer increased resolution for genetic mapping experiments and expand the pool of organisms amenable to genetic study. Using 88 markers distributed across 17 chromosomes, we analyze the introgression of chromosomal segments of Helianthus petiolaris into H. annuus in three natural hybrid zones. Introgression was significantly reduced relative to neutral expectations for 26 chromosomal segments, suggesting that each segment contains one or more factors that contribute to isolation. Pollen sterility is significantly associated with 16 of these 26 segments, providing a straightforward explanation of why this subset of blocks is disadvantageous in hybrids. In addition, comparison of rates of introgression across colinear vs. rearranged chromosomes indicates that close to 50% of the barrier to introgression is due to chromosomal rearrangements. These results demonstrate the utility of hybrid zones for identifying factors contributing to isolation and verify the prediction of increased resolution relative to controlled crosses.     

Polyphyly and gene flow between non-sibling Heliconius species

Background  

The view that gene flow between related animal species is rare and evolutionarily unimportant largely antedates sensitive molecular techniques. Here we use DNA sequencing to investigate a pair of morphologically and ecologically divergent, non-sibling butterfly species, Heliconius cydno and H. melpomene (Lepidoptera: Nymphalidae), whose distributions overlap in Central and Northwestern South America.     

Characteristic comparison between two types of miRNA precursors in metazoan species

MicroRNAs (miRNAs) are a class of small non-coding RNAs discovered in recent years, which are found to play important regulatory roles in various organisms. As the number of experimentally validated miRNAs is rapidly increasing, systematic analysis on the characteristics of these known miRNAs is necessary and indispensable, especially for computational prediction of new miRNAs. We extensively analyzed precursor sequences for all experimentally validated mature miRNAs in metazoan species, focusing on the characteristics at the level of primary sequences and secondary structures. An observation over the secondary structures of 2729 miRNA precursors (pre-miRNAs) reveals that these hairpin structures can be approximately classified into two types: one with a hairpin loop, and the other with multiple loops. Interestingly, the two types of pre-miRNAs show significant differences in both sequence and structure characteristics, and our study indicates that separate consideration on each type of pre-miRNAs is more reasonable, especially in computational prediction. Besides, we develop a new criterion called mAMFE which shows robust discriminative power in distinguishing pre-miRNAs against other RNAs, thus can potentially serve as a discriminative feature in prediction of new pre-miRNAs.     

Evidence for selection on a CONSTANS-like gene between two red oak species

Background and Aims

Hybridizing species such as oaks may provide a model to study the role of selection in speciation with gene flow. Discrete species'' identities and different adaptations are maintained among closely related oak species despite recurrent gene flow. This is probably due to ecologically mediated selection at a few key genes or genomic regions. Neutrality tests can be applied to identify so-called outlier loci, which demonstrate locus-specific signatures of divergent selection and are candidate genes for further study.

Methods

Thirty-six genic microsatellite markers, some with putative functions in flowering time and drought tolerance, and eight non-genic microsatellite markers were screened in two population pairs (n = 160) of the interfertile species Quercus rubra and Q. ellipsoidalis, which are characterized by contrasting adaptations to drought. Putative outliers were then tested in additional population pairs from two different geographic regions (n = 159) to support further their potential role in adaptive divergence.

Key Results

A marker located in the coding sequence of a putative CONSTANS-like (COL) gene was repeatedly identified as under strong divergent selection across all three geographically disjunct population pairs. COL genes are involved in the photoperiodic control of growth and development and are implicated in the regulation of flowering time.

Conclusions

The location of the polymorphism in the Quercus COL gene and given the potential role of COL genes in adaptive divergence and reproductive isolation makes this a promising candidate speciation gene. Further investigation of the phenological characteristics of both species and flowering time pathway genes is suggested in order to elucidate the importance of phenology genes for the maintenance of species integrity. Next-generation sequencing in multiple population pairs in combination with high-density genetic linkage maps could reveal the genome-wide distribution of outlier genes and their potential role in reproductive isolation between these species.     

A comparison of phenotypic plasticity between two species occupying different positions in a successional sequence

We compared the phenotypic plasticity of two greenhouse-grown species (Corispermum macrocarpum and Salsola collina) occupying different positions in a successional sequence in Horqin Sandy Land, by treating with different population density and the availability of soil nutrients and water. The same species can exhibit different patterns of plasticity in response to different environmental factors. In the soil nutrient treatments, the plasticity pattern of S. collina could be described as “master-of-some”. However, in the soil-water and population-density treatments, it showed no significant difference from C. macrocarpum in the reaction norm for plasticity. It was similar to a “jack-of-all-trades” plasticity pattern. Contrary to the previous conclusion that late successional species had higher reproductive allocation than early successional species, in this successional sequence, the late species had lower reproductive allocation in all treatments. Reproductive allocation of both species increased with the increase in water availability and also increased with a decrease in nutrient levels. However, density had no effect on reproductive allocation. Although the root:shoot ratio increased with decreasing water availability, there were no differences in the plasticity pattern for this trait in both species. Root:shoot ratio was, however, not significantly affected by nutrient availability and density. In a word, the plasticity patterns of invaders are adapted to the analyses of succession.     

Recent advances in assessing gene flow between diverging populations and species

The evolutionary process of divergence, which ultimately leads to the generation of new species, is thought to occur usually without any gene exchange between the diverging populations. However, until the recent growth of multi-locus datasets, and the development of new population genetic methods, it has been very difficult to assess whether or not closely related species have, or have not, exchanged genes during their divergence. Several recent studies have found significant signals of gene flow during species formation, calling into question the conventional wisdom that gene flow is absent during speciation.     

Water metabolism and the distribution of two species of australian murids,Rattus rattus and Rattus villosissimus

• 1.1. The ad libitum water requirement of Rattus villosissimus in the laboratory is significantly less than that of R. rattus. There are corresponding differences in the quantities of water eliminated via the urine, skin and lungs, although faecal water losses are similar.
• 2.2. R. rattus and R. villosissimus reduce body weight, urinary and faecal water loss, and probably food intake, when deprived of drinking water.
• 3.3. R. rattus is unable to limit body weight loss to the same degree as R. villosissimus when deprived of drinking water. This is partly due to inferior renal performance, although other factors such as higher evaporative water loss and lower food intake are probably involved.
• 4.4. The current distributions of R. rattus and R. villosissimus on the Australian mainland can be correlated with the known water metabolism of the two species.

     

Phenological comparison between two co-occurring Mediterranean woody species differing in growth form

Halimium atriplicifolium and Thymus vulgaris are two Mediterranean woody species, which differ in growth form and may co-occur under the same climatic constraints. Both possess distinct short (SS) and long shoots (LS). The aims of this work were: (1) to compare their phenological patterns, (2) to relate plant phenology with root depth and summer water potential, and (3) to compare the structure and phenology of SS and LS. Pre-dawn and mid-day shoot water potentials (Ψ_pd and Ψ_md) were assessed at the beginning and at the end of the driest period. SS and LS growth, flowering and fruit setting was followed every month throughout the annual cycle. Leaf shedding was followed with litter traps and leaf demography were monitored separately in SS and LS. Ψ_pd and Ψ_md exhibited a sharper drop in T. vulgaris than in H. atriplicifolium along the summer. Root depth of H. atriplicifolium was more than twice T. vulgaris. Phenophases of H. atriplicifolium occurred between spring and summer, while those of T. vulgaris concentrated in spring. The latter species shed many current-year leaves in September, probably in response to water shortage. In both species, LS growth occurred during a more rainy period than SS growth and during a warmer period in H. atriplicifolium. Leaf area and leaf mass per area were smaller for SS leaves than LS, probably due to water and carbon shortage at the time of SS growth. In conclusion, T. vulgaris suffered from more severe water stress than H. atriplicifilium due to its shallower root system and arrested phenological activity earlier in the summer. The different morphological and phenological traits of LS and SS suggest a specialisation in carbon gain along different time periods of the year.     

Manual lateralization in early primates: a comparison of two mouse lemur species

In humans, 90% of the population is right handed. Although population hand preference has been found in some primate species, the evolution of manual lateralization in primates is not yet clear. To gain insight into manual lateralization of ancestral primates, we studied hand usage in unspecialized quadrupedal, nocturnal lemurs, using a large sample size. We compared two closely related mouse lemur species to explore the variation of hand preference within the same genus. We tested 44 gray mouse lemurs and 19 Goodman's mouse lemurs in a forced food grasping task. The tests were videotaped. Measures of hand preference (i.e. the hand that is spontaneously chosen for a specific task) and successful hand usage (i.e. the hand that is successful in completing a specific task) were taken to explore manual lateralization. Both species showed manual lateralization at an individual, but not at a population level. Goodman's mouse lemurs showed stronger individual hand preferences than gray mouse lemurs. This suggests that strength in hand preference is variable within the same genus. No sex and age effects were found. The hand preference of offspring was negatively correlated to that of their mothers, but not correlated to that of their fathers. Thus, no clear genetic effect can be derived from these results. In the Goodman's mouse lemurs, hand preference increased with increasing task experience. However, successful hand usage was not affected by task experience, suggesting that successful hand usage is a more stable measurement for manual lateralization than hand preference.     

Genomic differentiation and patterns of gene flow between two long‐tailed tit species (Aegithalos)

Patterns of heterogeneous genomic differentiation have been well documented between closely related species, with some highly differentiated genomic regions (“genomic differentiation islands”) spread throughout the genome. Differential levels of gene flow are proposed to account for this pattern, as genomic differentiation islands are suggested to be resistant to gene flow. Recent studies have also suggested that genomic differentiation islands could be explained by linked selection acting on genomic regions with low recombination rates. Here, we investigate genomic differentiation and gene‐flow patterns for autosomes using RAD‐seq data between two closely related species of long‐tailed tits (Aegithalos bonvaloti and A. fuliginosus) in both allopatric and contact zone populations. The results confirm recent or ongoing gene flow between these two species. However, there is little evidence that the genomic regions that were found to be highly differentiated between the contact zone populations are resistant to gene flow, suggesting that differential levels of gene flow is not the cause of the heterogeneous genomic differentiation. Linked selection may be the cause of genomic differentiation islands between the allopatric populations with no or very limited gene flow, but this could not account for the heterogeneous genomic differentiation between the contact zone populations, which show evidence of recent or ongoing gene flow.     

Comparison of gene flow estimates between species of darters in different streams

Allozyme variation was assessed at two localities for 38 loci in Etheostoma blennioides and 43 loci in E. flabellare . Percent polymorphism (P) ranged from 18·4 to 31·6 and average heterozygosity (H) ranged from 0·026 to 0·079. Estimates of gene flow indicated panmictic populations of E. blennioides and sub-divided populations of E. flabellare , with significantly more substructuring of E. flabellare from one population. Population structuring of E. flabellare and no structuring of E. blennioides is consistent with predictions based on life history data. Significantly different gene flow estimates for E. flabellare between streams imply that each stream environment induced different population structures. Reduced heterozygosity for both species and significantly less population structuring in one population are consistent with drought-induced extinction and recolonization that probably occurs in the smaller stream.