Faster evolution of a premating reproductive barrier is not associated with faster speciation rates in New World passerine birds

Why are speciation rates so variable across the tree of life? One hypothesis is that this variation is explained by how rapidly reproductive barriers evolve. We tested this hypothesis by conducting a comparative study of the evolution of bird song, a premating barrier to reproduction. Speciation in birds is typically initiated when geographically isolated (allopatric) populations evolve reproductive barriers. We measured the strength of song as a premating barrier between closely related allopatric populations by conducting 2339 field experiments to measure song discrimination for 175 taxon pairs of allopatric or parapatric New World passerine birds, and estimated recent speciation rates from molecular phylogenies. We found evidence that song discrimination is indeed an important reproductive barrier: taxon pairs with high song discrimination in allopatry did not regularly interbreed in parapatry. However, evolutionary rates of song discrimination were not associated with recent speciation rates. Evolutionary rates of song discrimination were also unrelated to latitude or elevation, but species with innate song (suboscines) evolved song discrimination much faster than species with learned song (oscines). We conclude that song is a key premating reproductive barrier in birds, but faster evolution of this reproductive barrier between populations does not consistently result in faster diversification between species.

Reproductive Output and Insect Behavior in Hybrids and Apomicts from Limonium ovalifolium and L. binervosum Complexes (Plumbaginaceae) in an Open Cross-Pollination Experiment

Ex situ plant collections established from seeds of natural populations are key tools for understanding mating systems of intricate taxonomic complexes, as in the Limonium Mill. genus (sea lavenders, Plumbaginaceae). Plants show a polymorphic sexual system associated to flower polymorphisms such as ancillary pollen and stigma and/or heterostyly that prevents self and intramorph mating. The main objectives of this study were to investigate the significance of pollen-stigma dimorphisms and the role of flower visitors in the reproductive output of hybrids arising from sexual diploids of Limonium ovalifolium complex and apomicts tetraploids of L. binervosum complex in an open cross-pollination experiment. Results showed that, similarly to parental plants, hybrids present inflorescence types, self-incompatible flowers, and produced regular pollen grains with the typical exine patterns, with medium to high viability. By contrast, apomicts show floral polymorphisms, inflorescences, and pollen grains of maternal phenotype but with low stainability. Several insects’ species visited the inflorescences of parental plants and both hybrids and apomicts and some of these insects carried A and/or B pollen grains on their bodies, especially Clepsis coriacana (Rebel) and Tapinoma sp. Insects’ floral visits to hybrids and apomicts seem to be independent of pollen fertility and plants’ reproductive modes. Both hybrids and apomicts were able to produce fertile seeds, although the latter showed more seedlings with developmental anomalies than the first plants. The findings demonstrate that there is a weak reproductive barrier between the diploid species of L. ovalifolium complex as they can hybridize and produce fertile hybrids, provided there is pollen transport by pollinator insects. This study supports that apomixis is a strong reproductive barrier between both L. ovalifolium and L. binervosum complexes but did not allow us to exclude reproductive interferences of apomict pollen into sexuals.

Chemical signals act as the main reproductive barrier between sister and mimetic Heliconius butterflies

Colour pattern is the main trait that drives mate recognition between Heliconius species that are phylogenetically close. However, when this cue is compromised such as in cases of mimetic, sympatric and closely related species, alternative mating signals must evolve to ensure reproductive isolation and species integrity. The closely related species Heliconius melpomene malleti and H. timareta florencia occur in the same geographical region, and despite being co-mimics, they display strong reproductive isolation. In order to test which cues differ between species, and potentially contribute to reproductive isolation, we quantified differences in the wing phenotype and the male chemical profile. As expected, the wing colour pattern was indistinguishable between the two species, while the chemical profile of the androconial and genital males' extracts showed marked differences. We then conducted behavioural experiments to study the importance of these signals in mate recognition by females. In agreement with our previous results, we found that chemical blends and not wing colour pattern drive the preference of females for conspecific males . Also, experiments with hybrid males and females suggested an important genetic component for both chemical production and preference. Altogether, these results suggest that chemicals are the major reproductive barrier opposing gene flow between these two sister and co-mimic species.

Chemical signals act as the main reproductive barrier between sister and mimeticHeliconiusbutterflies

ABSTRACTColour pattern has been long recognised as the trait that drives mate recognition betweenHeliconiusspecies that are phylogenetically close. However, when this cue is compromised such as in cases of mimetic, sympatric and closely related species, alternative mating signals must evolve to ensure reproductive isolation and species integrity. The closely related speciesHeliconius melpomene malletiandH. timareta florencia, occur in the same geographic region and despite being co-mimics they display strong reproductive isolation. In order to test which cues differ between species, and therefore potentially contribute to reproductive isolation, we quantified differences in wing phenotype and male chemical profile. As expected, wing colour pattern was indistinguishable between the two species while the chemical profile of their male sex pheromones showed marked differences. We then conducted behavioural experiments to study the importance of these signals in mate recognition by females. In agreement with our previous results, we found that pheromones and not wing colour pattern drive the preference of females by conspecific males. In addition, experiments with hybrid males and females suggested an important genetic component for both pheromone production and preference. Altogether, these results suggest that pheromones are the major reproductive barrier opposing gene flow between these two sister and co-mimic species.

Centromere repositioning causes inversion of meiosis and generates a reproductive barrier

The chromosomal position of each centromere is determined epigenetically and is highly stable, whereas incremental cases have supported the occurrence of centromere repositioning on an evolutionary time scale (evolutionary new centromeres, ENCs), which is thought to be important in speciation. The mechanisms underlying the high stability of centromeres and its functional significance largely remain an enigma. Here, in the fission yeast Schizosaccharomyces pombe, we identify a feedback mechanism: The kinetochore, whose assembly is guided by the centromere, in turn, enforces centromere stability. Upon going through meiosis, specific inner kinetochore mutations induce centromere repositioning—inactivation of the original centromere and formation of a new centromere elsewhere—in 1 of the 3 chromosomes at random. Repositioned centromeres reside asymmetrically in the pericentromeric regions and cells carrying them are competent in mitosis and homozygotic meiosis. However, when cells carrying a repositioned centromere are crossed with those carrying the original centromere, the progeny suffer severe lethality due to defects in meiotic chromosome segregation. Thus, repositioned centromeres constitute a reproductive barrier that could initiate genetic divergence between 2 populations with mismatched centromeres, documenting a functional role of ENCs in speciation. Surprisingly, homozygotic repositioned centromeres tend to undergo meiosis in an inverted order—that is, sister chromatids segregate first, and homologous chromosomes separate second—whereas the original centromeres on other chromosomes in the same cell undergo meiosis in the canonical order, revealing hidden flexibility in the perceived rigid process of meiosis.

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 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 I. 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.Impact StatementBiological diversity depends on traits that prevent different species from successfully interbreeding. However, these reproductive barriers are often imperfect, leading to hybrid matings and possible genetic exchange between species where they occur together. When this happens, the reproductive barriers that separate species can themselves evolve to become stronger or weaker. Understanding the effects of hybridization on reproductive barriers is key to predicting the potential for future hybridization between species and ultimately whether hybridizing species will diverge, persist, or merge in regions where they co-occur. Here we hypothesize and show that hybridization in only one direction causes unidirectional changes to reproductive barrier strength and that geographically restricted hybridization causes local changes to barrier strength that can affect interbreeding within a species. Specifically, we found that gene flow from one species of morning glory into another likely caused a reproductive barrier to decrease in regions where they co-occur. The decreased reproductive barrier is caused by changes in only the species that received gene flow. We also found that the locally reduced barriers in the species that received gene flow affected reproductive compatibility between populations within that species. Thus, a breakdown of barriers between species can cause a build-up of barriers within a species. Our work demonstrates critical and rarely explored interactions at species boundaries.

Genome wide analysis of Ga1-s modifiers in maize

ABSTRACTA one way reproductive barrier exists between most popcorn varieties and dent corn varieties grown in the United States. This barrier is predominantly controlled by the ga1 locus. Using data from a diverse population of popcorn accessions pollinated by a dent corn tester, we found that the non-reciprocal pollination barrier conferred by ga1 is more complex than previously described. Individual accessions ranged from 0% to 100% compatible with dent corn pollen. Using conventional genotyping-by-sequencing data from 371 popcorn accessions carrying Ga1-s, seven significant modifiers of dent pollen compatibility were identified on five chromosomes. One locus may either be a nonfunctional ga1 allele present within popcorn, or second necessary gene for the reproductive barrier in genetic linkage with ga1, while the other modifiers are clearly genetically unlinked. The existence of ga1 modifiers segregating in a popcorn genetic background may indicate selective pressure to allow gene flow between populations, which should be incorporated into future models of the impact of genetic incompatibility loci on gene flow in natural and agricultural plant populations.

Parallel patterns of development between independent cases of hybrid seed inviability in Mimulus

SummaryRationaleHybrid seed inviability (HSI) is a common reproductive barrier in angiosperms, yet the evolutionary and developmental drivers of HSI remain largely unknown. We test whether conflict between maternal and paternal interests in resource allocation to developing offspring (i.e. parental conflict) are associated with HSI and determine the degree of developmental parallelism between independent incidences of HSI in Mimulus.MethodsWe quantified HSI between M. guttatus and two clades of M. decorus with oppositely asymmetric incompatibilities and surveyed development of hybrid and parental seeds.Key ResultsCrosses between M. guttatus and both clades of M. decorus show parent-of-origin effects on reciprocal F1 seed development, but in opposing directions. Inviable hybrid seeds exhibit paternal excess phenotypes, wherein endosperm is large and chaotic while viable hybrid seeds produce endosperm cells that are smaller and less prolific (i.e. maternal-excess phenotypes).Main ConclusionsWe find strong parent-of-origin effects on development in reciprocal F1s in multiple incidences of HSI in Mimulus. These patterns suggest that parental conflict may be an important force generating HSI in this group, and mismatches between maternal and paternal contributions to developing seeds result in repeatable developmental defects in hybrids.