Complex cross-incompatibility in morning glories is consistent with a role for mating system in plant speciation.

Reproductive isolation between selfing and outcrossing species can arise through diverse mechanisms, some of which are directly associated with differences in mating system. We dissected cross-incompatibility between the highly selfing morning glory Ipomoea lacunosa and its mixed-mating sister species Ipomoea cordatotriloba. We found that cross-incompatibility is complex, with contributions acting both before and after fertilization. We then investigated whether the transition in mating system may have facilitated the evolution of these reproductive barrier components through mismatched floral morphology, differences in reproductive context, or both. We found evidence that morphological mismatch likely contributes to reproductive isolation in at least one cross-direction and that other pollen-pistil interactions are present. We also identified hybrid seed inviability consistent with the predictions of the weak-inbreeder, strong-outbreeder hypotheses, suggesting endosperm misregulation plays an important role in cross-incompatibility. In contrast, we did not find evidence consistent with the prezygotic weak-inbreeder, strong-outbreeder hypothesis. Our study highlights the complexity of reproductive isolation between outcrossing and selfing species and the extent to which evolutionary consequences of mating system transitions can facilitate speciation.

Effects of the neo-X chromosome on genomic signatures of hybridization in Rumex hastatulus.

Natural hybrid zones provide opportunities for studies of the evolution of reproductive isolation in wild populations. Although recent investigations have found that the formation of neo-sex chromosomes is associated with reproductive isolation, the mechanisms remain unclear in most cases. Here, we assess the contemporary structure of gene flow in the contact zone between largely allopatric cytotypes of the dioecious plant Rumex hastatulus, a species with evidence of sex chromosome turn-over. Males to the west of the Mississippi river, USA, have an X and a single Y chromosome, whereas populations to the east of the river have undergone a chromosomal rearrangement giving rise to a larger X and two Y chromosomes. Using reduced-representation sequencing, we provide evidence that hybrids form readily and survive multiple backcross generations in the field, demonstrating the potential for ongoing gene flow between the cytotypes. Cline analysis of each chromosome separately captured no signals of difference in cline shape between chromosomes. However, principal component regression revealed a significant increase in the contribution of individual SNPs to inter-cytotype differentiation on the neo-X chromosome, but no correlation with recombination rate. Cline analysis revealed that the only SNPs with significantly steeper clines than the genome average were located on the neo-X. Our data are consistent with a role for neo-sex chromosomes in reproductive isolation between R. hastatulus cytotypes. Our investigation highlights the importance of studying plant hybrid zones for understanding the evolution of sex chromosomes.

Recombination landscape dimorphism and sex chromosome evolution in the dioecious plant Rumex hastatulus.

There is growing evidence from diverse taxa for sex differences in the genomic landscape of recombination, but the causes and consequences of these differences remain poorly understood. Strong recombination landscape dimorphism between the sexes could have important implications for the dynamics of sex chromosome evolution because low recombination in the heterogametic sex can favour the spread of sexually antagonistic alleles. Here, we present a sex-specific linkage map and revised genome assembly of Rumex hastatulus and provide the first evidence and characterization of sex differences in recombination landscape in a dioecious plant. We present data on significant sex differences in recombination, with regions of very low recombination in males covering over half of the genome. This pattern is evident on both sex chromosomes and autosomes, suggesting that pre-existing differences in recombination may have contributed to sex chromosome formation and divergence. Our analysis of segregation distortion suggests that haploid selection due to pollen competition occurs disproportionately in regions with low male recombination. We hypothesize that sex differences in the recombination landscape have contributed to the formation of a large heteromorphic pair of sex chromosomes in R. hastatulus, but more comparative analyses of recombination will be important to investigate this hypothesis further. This article is part of the theme issue 'Sex determination and sex chromosome evolution in land plants'.

Modularity and selection of nectar traits in the evolution of the selfing syndrome in Ipomoea lacunosa (Convolvulaceae).

Although the evolution of the selfing syndrome often involves reductions in floral size, pollen and nectar, few studies of selfing syndrome divergence have examined nectar. We investigate whether nectar traits have evolved independently of other floral size traits in the selfing syndrome, whether nectar traits diverged due to drift or selection, and the extent to which quantitative trait locus (QTL) analyses predict genetic correlations. We use F5 recombinant inbred lines (RILs) generated from a cross between Ipomoea cordatotriloba and Ipomoea lacunosa. We calculate genetic correlations to identify evolutionary modules, test whether trait divergence was due to selection, identify QTLs and perform correlation analyses to evaluate how well QTL properties reflect genetic correlations. Nectar and floral size traits form separate evolutionary modules. Selection has acted to reduce nectar traits in the selfing I. lacunosa. Genetic correlations predicted from QTL properties are consistent with observed genetic correlations. Changes in floral traits associated with the selfing syndrome reflect independent evolution of at least two evolutionary modules: nectar and floral size traits. We also demonstrate directional selection on nectar traits, which is likely to be independent of selection on floral size traits. Our study also supports the expected mechanistic link between QTL properties and genetic correlations.

Genetic architecture of divergence: the selfing syndrome in Ipomoea lacunosa.

PREMISE: Highly selfing plant species frequently display a distinctive suite of traits termed the selfing syndrome. Here we tested the hypothesis that these traits are grouped into correlated evolutionary modules and determined the degree of independence between such modules. METHODS: We evaluated phenotypic correlations and QTL overlaps in F2 offspring of a cross between the morning glories Ipomoea lacunosa and I. cordatotriloba and investigated how traits clustered into modules at both the phenotypic and genetic level. We then compared our findings to other QTL studies of the selfing syndrome. RESULTS: In the I. lacunosa selfing syndrome, traits grouped into modules that displayed correlated evolution within but not between modules. QTL overlap predicted phenotypic correlations, and QTLs affecting the same trait module were significantly physically clustered in the genome. The genetic architecture of the selfing syndrome varied across systems, but the pattern of stronger within- than between-module correlation was widespread. CONCLUSIONS: The genetic architecture we observe in the selfing syndrome is consistent with a growing understanding of floral morphological integration achieved via pleiotropy in clustered traits. This view of floral evolution is consistent with resource limitation or predation driving the evolution of the selfing syndrome, but invites further research into both the selective causes of the selfing syndrome and how genetic architecture itself evolves in response to changes in mating system.

Morning glory species co-occurrence is associated with asymmetrically decreased and cascading reproductive isolation.

Hybridization between species can affect the strength of the reproductive barriers that separate those species. Two extensions of this effect are (1) the expectation that asymmetric hybridization or gene flow will have asymmetric effects on reproductive barrier strength and (2) the expectation that local hybridization will affect only local reproductive barrier strength and could therefore alter within-species compatibility. We tested these hypotheses in a pair of morning glory species that exhibit asymmetric gene flow from highly selfing Ipomoea lacunosa into mixed-mating Ipomoea cordatotriloba in regions where they co-occur. Because of the direction of this gene flow, we predicted that reproductive barrier strength would be more strongly affected in I. cordatotriloba than I. lacunosa. We also predicted that changes to reproductive barriers in sympatric I. cordatotriloba populations would affect compatibility with allopatric populations of that species. We tested these predictions by measuring the strength of a reproductive barrier to seed set across the species' ranges. Consistent with our first prediction, we found that sympatric and allopatric I. lacunosa produce the same number of seeds in crosses with I. cordatotriloba, whereas crosses between sympatric I. cordatotriloba and I. lacunosa are more successful than crosses between allopatric I. cordatotriloba and I. lacunosa. This difference in compatibility appears to reflect an asymmetric decrease in the strength of the barrier to seed set in sympatric I. cordatotriloba, which could be caused by I. lacunosa alleles that have introgressed into I. cordatotriloba. We further demonstrated that changes to sympatric I. cordatotriloba have decreased its ability to produce seeds with allopatric populations of the same species, in line with our second prediction. Thus, in a manner analogous to cascade reinforcement, we suggest that introgression associated with hybridization not only influences between-species isolation but can also contribute to isolation within a species.

Widespread Recombination Suppression Facilitates Plant Sex Chromosome Evolution.

Classical models suggest that recombination rates on sex chromosomes evolve in a stepwise manner to localize sexually antagonistic variants in the sex in which they are beneficial, thereby lowering rates of recombination between X and Y chromosomes. However, it is also possible that sex chromosome formation occurs in regions with preexisting recombination suppression. To evaluate these possibilities, we constructed linkage maps and a chromosome-scale genome assembly for the dioecious plant Rumex hastatulus. This species has a polymorphic karyotype with a young neo-sex chromosome, resulting from a Robertsonian fusion between the X chromosome and an autosome, in part of its geographic range. We identified the shared and neo-sex chromosomes using comparative genetic maps of the two cytotypes. We found that sex-linked regions of both the ancestral and the neo-sex chromosomes are embedded in large regions of low recombination. Furthermore, our comparison of the recombination landscape of the neo-sex chromosome to its autosomal homolog indicates that low recombination rates mainly preceded sex linkage. These patterns are not unique to the sex chromosomes; all chromosomes were characterized by massive regions of suppressed recombination spanning most of each chromosome. This represents an extreme case of the periphery-biased recombination seen in other systems with large chromosomes. Across all chromosomes, gene and repetitive sequence density correlated with recombination rate, with patterns of variation differing by repetitive element type. Our findings suggest that ancestrally low rates of recombination may facilitate the formation and subsequent evolution of heteromorphic sex chromosomes.

Evolutionary Genomics of Plant Gametophytic Selection.

It has long been recognized that natural selection during the haploid gametophytic phase of the plant life cycle may have widespread importance for rates of evolution and the maintenance of genetic variation. Recent theoretical advances have further highlighted the significance of gametophytic selection for diverse evolutionary processes. Genomic approaches offer exciting opportunities to address key questions about the extent and effects of gametophytic selection on plant evolution and adaptation. Here, we review the progress and prospects for integrating functional and evolutionary genomics to test theoretical predictions, and to examine the importance of gametophytic selection on genetic diversity and rates of evolution. There is growing evidence that selection during the gametophyte phase of the plant life cycle has important effects on both gene and genome evolution and is likely to have important pleiotropic effects on the sporophyte. We discuss the opportunities to integrate comparative population genomics, genome-wide association studies, and experimental approaches to further distinguish how differential selection in the two phases of the plant life cycle contributes to genetic diversity and adaptive evolution.

Multiple aspects of the selfing syndrome of the morning glory Ipomoea lacunosa evolved in response to selection: A Qst-Fst comparison.

The frequent transition from outcrossing to selfing in flowering plants is often accompanied by changes in multiple aspects of floral morphology, termed the "selfing syndrome." While the repeated evolution of these changes suggests a role for natural selection, genetic drift may also be responsible. To determine whether selection or drift shaped different aspects of the pollination syndrome and mating system in the highly selfing morning glory Ipomoea lacunosa, we performed multivariate and univariate Qst-Fst comparisons using a wide sample of populations of I. lacunosa and its mixed-mating sister species Ipomoea cordatotriloba. The two species differ in early growth, floral display, inflorescence traits, corolla size, nectar, and pollen number. Our analyses support a role for natural selection driving trait divergence, specifically in corolla size and nectar traits, but not in early growth, display size, inflorescence length, or pollen traits. We also find evidence of selection for reduced herkogamy in I. lacunosa, consistent with selection driving both the transition in mating system and the correlated floral changes. Our research demonstrates that while some aspects of the selfing syndrome evolved in response to selection, others likely evolved due to drift or correlated selection, and the balance between these forces may vary across selfing species.

Gene flow, divergent selection and resistance to introgression in two species of morning glories (Ipomoea).

Gene flow is thought to impede genetic divergence and speciation by homogenizing genomes. Recent theory and research suggest that sufficiently strong divergent selection can overpower gene flow, leading to loci that are highly differentiated compared to others. However, there are also alternative explanations for this pattern. Independent evidence that loci in highly differentiated regions are under divergent selection would allow these explanations to be distinguished, but such evidence is scarce. Here, we present multiple lines of evidence that many of the highly divergent SNPs in a pair of sister morning glory species, Ipomoea cordatotriloba and I. lacunosa, are the result of divergent selection in the face of gene flow. We analysed a SNP data set across the genome to assess the amount of gene flow, resistance to introgression and patterns of selection on loci resistant to introgression. We show that differentiation between the two species is much lower in sympatry than in allopatry, consistent with interspecific gene flow in sympatry. Gene flow appears to be substantially greater from I. lacunosa to I. cordatotriloba than in the reverse direction, resulting in sympatric and allopatric I. cordatotriloba being substantially more different than sympatric and allopatric I. lacunosa. Many SNPs highly differentiated in allopatry have experienced divergent selection, and, despite gene flow in sympatry, resist homogenization in sympatry. Finally, five out of eight floral and inflorescence characteristics measured exhibit asymmetric convergence in sympatry. Consistent with the pattern of gene flow, I. cordatotriloba traits become much more like those of I. lacunosa than the reverse. Our investigation reveals the complex interplay between selection and gene flow that can occur during the early stages of speciation.

Do animals living in larger groups experience greater parasitism? A meta-analysis.

Parasitism is widely viewed as the primary cost of sociality and a constraint on group size, yet studies report varied associations between group size and parasitism. Using the largest database of its kind, we performed a meta-analysis of 69 studies of the relationship between group size and parasite risk, as measured by parasitism and immune defenses. We predicted a positive correlation between group size and parasitism with organisms that show contagious and environmental transmission and a negative correlation for searching parasites, parasitoids, and possibly vector-borne parasites (on the basis of the encounter-dilution effect). Overall, we found a positive effect of group size (r = 0.187) that varied in magnitude across transmission modes and measures of parasite risk, with only weak indications of publication bias. Among different groups of hosts, we found a stronger relationship between group size and parasite risk in birds than in mammals, which may be driven by ecological and social factors. A metaregression showed that effect sizes increased with maximum group size. Phylogenetic meta-analyses revealed no evidence for phylogenetic signal in the strength of the group size-parasitism relationship. We conclude that group size is a weak predictor of parasite risk except in species that live in large aggregations, such as colonial birds, in which effect sizes are larger.

Evolution of sexual dimorphism in bill size and shape of hermit hummingbirds (Phaethornithinae): a role for ecological causation.

Unambiguous examples of ecological causation of sexual dimorphism are rare, and the best evidence involves sexual differences in trophic morphology. We show that moderate female-biased sexual dimorphism in bill curvature is the ancestral condition in hermit hummingbirds (Phaethornithinae), and that it is greatly amplified in species such as Glaucis hirsutus and Phaethornis guy, where bills of females are 60 per cent more curved than bills of males. In contrast, bill curvature dimorphism is lost or reduced in a lineage of short-billed hermit species and in specialist Eutoxeres sicklebill hermits. In the hermits, males tend to be larger than females in the majority of species, although size dimorphism is typically small. Consistent with earlier studies of hummingbird feeding performance, both raw regressions of traits and phylogenetic independent contrasts supported the prediction that dimorphism in bill curvature of hermits is associated with longer bills. Some evidence indicates that differences between sexes of hermit hummingbirds are associated with differences in the use of food plants. We suggest that some hermit hummingbirds provide model organisms for studies of ecological causation of sexual dimorphism because their sexual dimorphism in bill curvature provides a diagnostic clue for the food plants that need to be monitored for studies of sexual differences in resource use.