A genome-wide survey of reproductive barriers in an intraspecific hybrid

Genetic study of the reproductive barriers between related species plays an essential role in understanding the process of speciation. We developed a new method for mapping all possible factors causing deviations from expected Mendelian segregation ratios in F(2) progeny, which substantially contribute to reproductive isolation. A multiresponse nonlinear regression analysis of the allele frequencies of the markers covering an entire genome in the F(2) population was performed to estimate the map position and intensity of the reproductive barriers on each chromosome. In F(2) plants from a cross between a Japonica variety of rice, Nipponbare, and an Indica variety, Kasalath, the deviations of allele frequencies were well explained by 33 reproductive barriers. Of these, 15 reproductive barriers affected the allele transmission rate through the gametophyte and in 9 of these 15 cases, an Indica allele was transmitted at a higher frequency than a Japonica allele. The other 18 reproductive barriers altered the viability of the zygote via its genotype. Two zygotic reproductive barriers showed overdominance and 5 showed underdominance. The most pronounced reproductive barrier, mapped at 62.3 +/- 0.4 cM on chromosome 3, transmitted the Indica allele by 94% through the male gametophyte. The accuracy of the barrier position in the regression analysis was confirmed by progeny analysis. The regression analysis proved to be a powerful tool for detecting and characterizing every reproductive barrier, irrespective of whether it acted on the male or female gametophyte or the zygote.     

Diverse reproductive barriers in hybridising crickets suggests extensive variation in the evolution and maintenance of isolation

Reproductive barriers reduce gene flow between populations and maintain species identities. A diversity of barriers exist, acting before, during and after mating. To understand speciation and coexistence, these barriers need to be quantified and their potential interactions revealed. We use the hybridising field crickets Gryllus bimaculatus and G. campestris as a model to understand the full compliment and relative strength of reproductive barriers. We find that males of both species prefer conspecific females, but the effect is probably too weak to represent a barrier. In contrast, prezygotic barriers caused by females being more attracted to conspecific male song and preferentially mounting and mating with conspecifics are strong and asymmetric. Postzygotic barriers vary in direction; reductions in fecundity and egg viability create selection against hybridisation, but hybrids live longer than pure-bred individuals. Hybrid females show a strong preference for G. bimaculatus songs, which together with a complete lack of hybridisation by G. campestris females, suggests that asymmetric gene flow is likely. For comparison, we review reproductive barriers that have been identified between other Gryllids and conclude that multiple barriers are common. Different species pairs are separated by qualitatively different combinations of barriers, suggesting that reproductive isolation and even the process of speciation itself may vary widely even within closely related groups.     

Relationship between transmission ratio distortion and genetic divergence in intraspecific rice crosses

The strength of reproductive isolation often correlates positively with parental divergence in both animals and plants. Here, we assess the relationship between transmission ratio distortion (TRD) of marker loci and parental divergence in intraspecific rice (Oryza sativa L.) crosses. We produced 10 diverse F(2) populations by crossing a temperate japonica reference accession with each of 10 donor accessions belonging to subpopulations different from the reference accession, and then genotyped the F(2) populations using molecular markers distributed across the entire genome. Significant TRDs (α?=?0.05) were detected in 9 of the 10 F(2) populations. TRD regions on chromosomes 3 and 6 were common to several populations; in contrast, other TRD regions were unique to a single population, indicating the diversification of genomic location of TRDs among the populations. The level of TRD (estimated from the overall number and magnitude of TRDs) was significantly correlated with the genetic distance between the donor accessions and the reference accession. Our results suggest that in intraspecific rice crosses, parental divergence may result in diversification of the TRD pattern, followed by an increase in the level of TRD.     

A resource budget model to explain intraspecific variation in mast reproductive dynamics

Rowan, Sorbus aucuparia L., exhibits conspicuous geographic variation in its inter-annual patterns of reproduction across southern Norway. Along the southern west coast, trees flower and produce clusters of succulent berries every other year, while in the east, trees mast every 3 years. We investigate two hypotheses for this variation: local adaptation to environmental conditions that favors different reproductive schedules at different locations or variation arising from single stereotyped reproductive strategy in the face of a geographic variation in productivity. To assess the theoretical plausibility of each of these hypotheses, we develop a refined resource budget model for mast reproduction. The refined model assumes that there is a lower bound on the amount of resource that may be allocated to reproduction, which allows the prediction of the relation between reproductive schedules and productivity. From the analysis of the model, we find that the observed geographic transition in rowan mast is caused if either productivity in the east is lower than that in the west or if plants in the eastern populations have evolved to pause reproduction until energy reserves are replenished to higher levels. The prediction by the productivity gradient hypothesis match with the empirical finding that the productivity is, in fact, likely to be lower in the east than the west, although we lack empirical data to test the likelihood of the local adaptation hypothesis. There is a need for experimental studies to clarify the validity of the local adaptation hypothesis. Akiko Satake is the recipient of the 11th Denzaburo Miyadi Award.     

Effects of intraspecific competition on size variation and reproductive allocation in a clonal plant

Clonal plants grow in diameter rather than height, and therefore competition among genets is likely to be symmetric and to result in smaller variation in size of genets than in non-clonal plants. Moreover, clonal plants can reproduce both sexually and vegetatively. We studied the effects of density on the size of rosettes and of clones, variation in the size of rosettes and of clones, and allocation to sexual and vegetative reproduction in the clonal herb Ranunculus reptans . We grew plants from an artificial population of R. reptans in 32 trays at two densities. After four months, differences in density were still apparent, although clones in the low-density treatment had on average 155% more rosettes and 227% more rooted rosettes than clones in the high-density treatment. The coefficient of variation of these measures of clone size was 15% and 83% higher, respectively, in the low-density treatment. This indicates that intraspecific competition among clones of R. reptans is symmetric and increases the effective population size. Rooted rosettes were larger and varied more in size in the low-density treatment. The relative allocation of the populations to sexual and to vegetative reproduction was 19% and 13% higher, respectively, in the high-density treatment. Moreover, seeds produced in the high-density treatment had a 24% higher mass and a 7% higher germination percentage. This suggests that with increasing density, allocation to sexual reproduction increases more than allocation to vegetative reproduction in R. reptans , which corresponds to the response of some other species with a spreading growth form but not of species with a compact growth form. We conclude that intraspecific competition is an important factor in the life-history evolution of R. reptans because intraspecific competition affects its clonal life-history traits and may affect evolutionary processes such as genetic drift and selection through its effect on the effective population size.     

Site variation in reproductive synchrony in three neotropical figs

Abstract. To investigate the persistence of figs and their short-lived pollinators in highly seasonal environments and in small populations, three native figs were studied near the edge of their range in Sonora, Mexico. The reproductive phenologies of Ficus insipida (Willd.) and F. petiolaris (H.B.K.) were contrasted between a drier site with small populations and a wetter site with large populations. In addition, F. pertusa (L.) phenology was censused in the wetter site and compared with findings from Central America. Trees from smaller populations in the drier site produced less synchronous crops. Individuals within populations became reproductively synchronized at the population level but rapidly attained asynchrony in the drier site because of a breakdown in within-tree crop synchrony. Sexual-phase overlap occurred in all species and sites. Intraspecific variation in reproductive phenology may explain the persistence of figs and fig wasps in highly seasonal environments and small populations.     

Intraspecific variation in reproductive barriers between two closely related Arabidopsis sister species

Reproductive isolation (RI) is a critical component of speciation and varies strongly in timing and strength among different sister taxa, depending on, for example the geography of speciation and divergence time. However, these factors may also produce variation in timing and strength among populations within species. Here we tested for variation in the expression of RI among replicate population pairs between the sister taxa Arabidopsis lyrata subsp. lyrata and A. arenicola. While the former is predominantly outcrossing, the latter is predominantly selfing. We focused on intrinsic prezygotic and postzygotic RI as both species occur largely in allopatry. We assessed RI by performing within-population crosses and interspecific between-population crosses, and by raising offspring. RI was generally high between all interspecific population pairs, but it varied in timing and strength depending on population history. Prezygotic isolation was strongest between the closest-related population pair, while early postzygotic isolation was high for all other population pairs. Furthermore, the timing and strength of RI depended strongly on cross direction. Our study provides empirical support that reproductive barriers between species are highly variable among population pairs and asymmetric within population pairs, and this variation seems to follow patterns typically described across species pairs.     

Reciprocal crosses between Magnolia stellata and Magnolia kobus do not show significant reproductive barriers in seed formation

Congeneric invasive species reduce genetic endemism of native species through hybridization and sometimes cause extinction through genetic or demographic swamping. In the range of Magnolia stellata, a native rare subtree species, Magnolia kobus, an invasive planted/escaped tree species, can also be found. In order to examine possible natural hybridization between the two species, a reciprocal cross-pollination experiment was conducted, and fruit set, seed set, female reproductive success in seed formation (FRS; fruit set × seed set) and seed weight were estimated. With M. stellata as the maternal tree, there were no significant differences in all measurements between intra- and interspecific crosses. With M. kobus as the maternal tree, there were also no significant differences in all measurements except fruit set. These results suggest that there are no reproductive barriers between the two species and planted/escaped M. kobus near the natural habitat of M. stellata presents a threat through hybridization.     

Genome-wide intraspecific DNA-sequence variations in rice

Genome-wide comparative analysis of the DNA sequences of two major cultivated rice subspecies, Oryza sativa L. ssp indica and Oryza sativa L. ssp japonica, have revealed their extensive microcolinearity in gene order and content. However, deviations from colinearity are frequent owing to insertions or deletions. Intraspecific sequence polymorphisms commonly occur in both coding and non-coding regions. These variations often affect gene structures and may contribute to intraspecific phenotypic adaptations.     

Comparison of single seed descent and anther culture-derived lines of three single crosses of rice

Summary Distribution parameters (mean, variance, skewness and kurtosis) of 12 quantitative traits were evaluated for inbred lines generated through single seed descent (SSD) and anther culture (AC) of two japonica x japonica hybrids and one japonica x indica hybrid of rice. For most of the traits the data were normally distributed, and the means and variances were found to be identical for SSD- and AC-derived lines of the given hybrids. However, for some other traits, differences between the two population types were observed, mainly in the lines derived from the intra-japonica crosses. A tentative explanation for these differences is given. Nevertheless, our results suggest that SSD and AC are equally effective breeding techniques for producing agronomically useful lines of rice.     

Three representative inter and intra‐subspecific crosses reveal the genetic architecture of reproductive isolation in rice

Systematic characterization of genetic and molecular mechanisms in the formation of hybrid sterility is of fundamental importance in understanding reproductive isolation and speciation. Using ultra‐high‐density genetic maps, 43 single‐locus quantitative trait loci (QTLs) and 223 digenic interactions for embryo‐sac, pollen, and spikelet fertility are depicted from three crosses between representative varieties of japonica and two varietal groups of indica, which provide an extensive archive for investigating the genetic basis of reproductive isolation in rice. Ten newly detected single‐locus QTLs for inter‐ and intra‐subspecific fertility are identified. Three loci for embryo‐sac fertility are detected in both Nip × ZS97 and Nip × MH63 crosses, whereas QTLs for pollen fertility are not in common between the two crosses thus leading to fertility variation. Five loci responsible for fertility and segregation distortion are observed in the ZS97 × MH63 cross. The importance of two‐locus interactions on fertility are quantified in the whole genome, which identify that three types of interaction contribute to fertility reduction in the hybrid. These results construct the genetic architecture with respect to various forms of reproductive barriers in rice, which have significant implications in utilization of inter‐subspecific heterosis along with improvement in the fertility of indica–indica hybrids at single‐ and multi‐locus level.     

Inter- and intraspecific variation in the life histories of three sympatric isopods in a Hong Kong forest

There is a paucity of data on the life-history strategies of tropical animals. Accordingly, the inter and intraspecific life-history variations of three sympatric isopods, Burmoniscus oceliutus (Philosciidae), Formosillo raffaelei and Orodillo maculatus (Armadillidae), were studied at two sites in a Hong Kong forest. All three isopods were iteroparous. Burmoniscus oceilutus had more frequent breeding bouts, and smaller broods than O. muculutus and F. raffaelei. Although the three isopods had different life spans, brood numbers and life-time fecundities, their rates of offspring production (number of eggs per month) were similar. The Hong Kong isopods had longer breeding periods, a greater number of broods per life time, and lower reproductive allocation per brood than their temperate counterparts. These findings were consistent with the predictions of r - and K-theory. Intraspecific, between-site differences in fecundity and brood dry weight of F. raffaelei could probably be explained by the variations in the size of gravid females. Burmoniscus ocellutus produced heavier eggs at the site with a higher population density, suggesting that conditions at the site with a higher isopod density may be more K-selecting. Female-biased sex ratios, possibly resulting from differential sex-specific mortality, were common among the isopod samples, and the possible adaptive significance of this pattern was discussed. The potential influence of phylogenetic constraints on the evolution of life-history strategies was also considered.     

Evaluating intraspecific variation in insect trait analysis

1. Intraspecific variation plays important roles in ecology and evolution. Yet, information on how species and populations vary remains scarce, particularly for insects and regarding functional traits. This lack of knowledge can be problematic in trait‐based ecology because traditional approaches assume negligible intraspecific variation, even for analyses that assess highly variable taxa.
2. We measured 291 Arctic fritillary butterflies (Boloria chariclea) to assess the intraspecific variation in one population of this species, evaluating (i) how wingspan of Arctic fritillaries varies in relation to the other species of its community, and (ii) how well wingspan, a measure of body size, predicts weight, a measure of body mass.
3. Wingspan of Arctic fritillaries varied between 2.62 and 4.07 cm, with the 95% interval range, including ～33% (14/42) of the species in the community, and ～30% (84/279) of the butterflies of Canada. The relationship between wingspan and weight was significant (β_wingspan = 0.002, SE = 0.0008, P < 0.001), but relatively weak (R²_adj = 0.31, F_2,288 = 67.82, P < 0.001).
4. We discuss our findings in relation to the assumption of species homogeneity and the use of proxies in the analysis of species traits, complementing our case study with simulations to illustrate how intraspecific and interspecific variation interact in determining when traditional trait analyses are robust. We suggest entomologists interested in trait analyses should critically evaluate how intraspecific variation could affect their inference, especially when evaluating species that are highly sexually dimorphic, phenotypically plastic, and/or distributed across broad environmental and spatial clines.

     

The evolution of intraspecific variation in social organization

Many species show intraspecific variation in their social organization (IVSO), which means the composition of their social groups can change between solitary living, pair living, or living in groups. Understanding IVSO is important because it demonstrates species resilience to environmental change and can help us to study ultimate and proximate reasons for group living by comparing solitary and group‐living individuals in a single species. It has long been realized that the environment plays a key role in explaining the occurrence of IVSO. IVSO is expected to have evolved in variable environments and can thus be a key adaptation to environmental change. It has previously been suggested that four different mechanisms relying on the environment exist that can lead to IVSO: environmental disrupters, genetic differentiation, developmental plasticity, and social flexibility. All four mechanisms depend on the environment such that focusing only on environmental factors alone cannot explain IVSO. Importantly, only three represent evolved mechanisms, while environmental disrupters leading to the death of important group members induce nonadaptive IVSO. Environmental disrupters can be expected to cause IVSO even in species where IVSO is also an adaptive response. Here, we focus on the questions of why IVSO occurs and why it evolved. To understand IVSO at the species level, it is important to conduct continuous long‐term studies to differentiate between nonadaptive and adaptive IVSO. We predict that IVSO evolves in environments that vary in important ecological variables, such as rainfall, food availability, and population density. IVSO might also depend on life history factors, especially longevity. IVSO is predicted to be more common in species with a short life span and that breed only for one breeding season, being selected to respond optimally to the prevailing environmental situation. Finally, we emphasize the importance of accounting for IVSO when studying social evolution, especially in comparative studies, as not every species can be assigned to one single form of social organization. For such comparative studies, it is important to use data based on the primary literature.     

Prezygotic barriers to hybridization in marine broadcast spawners: reproductive timing and mating system variation

Sympatric assemblages of congeners with incomplete reproductive barriers offer the opportunity to study the roles that ecological and non-ecological factors play in reproductive isolation. While interspecific asynchrony in gamete release and gametic incompatibility are known prezygotic barriers to hybridization, the role of mating system variation has been emphasized in plants. Reproductive isolation between the sibling brown algal species Fucus spiralis, Fucus guiryi (selfing hermaphrodite) and Fucus vesiculosus (dioecious) was studied because they form hybrids in parapatry in the rocky intertidal zone, maintain species integrity over a broad geographic range, and have contrasting mating systems. We compared reproductive synchrony (spawning overlap) between the three species at several temporal scales (yearly/seasonal, semilunar/tidal, and hourly during single tides). Interspecific patterns of egg release were coincident at seasonal (single peak in spring to early summer) to semilunar timescales. Synthesis of available data indicated that spawning is controlled by semidiurnal tidal and daily light-dark cues, and not directly by semilunar cycles. Importantly, interspecific shifts in timing detected at the hourly scale during single tides were consistent with a partial ecological prezygotic hybridization barrier. The species displayed patterns of gamete release consistent with a power law distribution, indicating a high degree of reproductive synchrony, while the hypothesis of weaker selective constraints for synchrony in selfing versus outcrossing species was supported by observed spawning in hermaphrodites over a broader range of tidal phase than in outcrossers. Synchronous gamete release is critical to the success of external fertilization, while high-energy intertidal environments may offer only limited windows of reproductive opportunity. Within these windows, however, subtle variations in reproductive timing have evolved with the potential to form ecological barriers to hybridization.     

Ecological consequences of intraspecific variation in lake Daphnia

1. Although populations harbour considerable diversity, most ecological studies still assume they are homogeneous. However, mounting evidence suggests that intraspecific diversity is not only common, but also important for interactions with community members. Here, intraspecific variation in Daphnia dentifera in haemoglobin content is shown to be a marker of hypolimnion use. 2. Hypolimnion use differed substantially within and among D. dentifera populations. Daphnia dentifera with haemoglobin resided primarily in the hypolimnion, while D. dentifera lacking haemoglobin migrated vertically. These ‘deep’ and ‘migratory’D. dentifera had different seasonal phenologies and dynamics. 3. Deep and migratory D. dentifera had qualitatively different relationships with an important competitor, Daphnia pulicaria. Deep D. dentifera density was negatively correlated with D. pulicaria density, whereas migratory density was not correlated with D. pulicaria density. 4. Given that D. pulicaria tends to reside in the hypolimnion, this negative correlation probably reflects competition between D. pulicaria and the deep D. dentifera. This pattern would have been missed if only the relationship between the overall lake populations of D. dentifera and D. pulicaria had been studied. 5. Abundances of deep D. dentifera and D. pulicaria were both correlated with the size of the hypolimnetic refuge from fish predation, but in opposite directions. Lakes with large refuges generally had high D. pulicaria and low deep D. dentifera densities.     

Interspecific and intraspecific variation in the performance of three pest aphid species on five grain legume hosts

The suitability of five grain legume species (narrow-leafed lupin, chickpea, faba bean, field pea, lentil) as hosts for three aphid species (green peach aphid, cowpea aphid, bluegreen aphid) was evaluated by measuring the mean relative growth rate (MRGR) and survivorship of nymphs over a 5 day period. For each aphid species, intraspecific (interclonal) variation was also determined by independently measuring the performance of 30 clones collected from a variety of hosts and from different parts of the Western Australia (WA) wheatbelt. The suitability of the grain legumes varied among aphid species. Chickpea was not a suitable host for any of the aphids tested. Averaged over all clones, lentil and faba bean were the most suitable hosts for cowpea aphid, and narrow-leafed lupin was the most suitable host for green peach aphid. Field pea was a suitable host for all three species, but only at a suboptimal level. Cowpea aphid showed the greatest amount of intraspecific variation, with significant variation in MRGR among clones on all hosts except chickpea and significant variation in survivorship on chickpea and lupin. For green peach aphid, there was significant variation in MRGR among clones on field pea and lupin, but in survivorship on lupin only. Bluegreen aphid clones showed significant variation only for MRGR on faba bean and lupin. There were positive correlations in performance of green peach aphid clones on faba bean and lentil, and of cowpea aphid clones on faba bean and lentil. Bluegreen aphid clones showed a negative correlation in performance on field pea and faba bean. These results show the importance of screening cultivars against a wide variety of aphid clones when assessing aphid susceptibility in breeding programmes. The implications of these results on the adaptability of parthenogenetic aphids are discussed.