Immigrant Inviability Research Articles

The role of mycorrhizal fungi in driving ecotype formation in mycoheterotrophic plants

In his seminal paper, Göte Turesson proposed the term ecotype as the ‘ecological unit to cover the product arising as a result of the genotypical response of an ecospecies to a particular habitat'. Turesson further outlined that to fully understand the ecology of a species, a knowledge of its most important ecotypes is needed. Whereas Turesson's original idea of an ecotype mainly referred to the response of a species to abiotic conditions, there is mounting evidence that ecotypes can also originate as a response to biotic conditions. Hence, to understand the ecology of a species, one should also understand the distribution and variation in biotic interactions. For plants, one such biotic interaction involves mycorrhizal fungi. Particularly in mycoheterotrophic plants, i.e. plants that rely on mycorrhizal fungi for their carbon supply, adaptation to and specialization on mycorrhizal fungi have the potential to drive ecotype formation and speciation. In this paper, we provide evidence that populations of mycoheterotrophic plants inhabiting contrasting habitats commonly encounter divergent mycorrhizal fungal communities leading to geographic mosaics of mycorrhizal interactions. Adaptation to local fungal communities, in turn, can induce (partial) reproductive isolation and contribute to ecotype and ultimately species formation as a result of decreased fitness of immigrant genotypes (immigrant inviability). In the most extreme case, loss of photosynthesis and mycorrhizal switching have led to reproductive isolation and the development of novel species that have become fully mycoheterotrophic. Such shifts have occurred repeatedly during the evolutionary history of land plants. We conclude that mycorrhizal fungi not only contribute to the early divergence of populations of mycoheterotrophic plants, but also play a crucial role in the further diversification and origination of this unique set of species that rely on mycorrhizal fungi for obtaining carbon and completing their life cycle.

Genomic signatures of adaptive divergence in lacustrine copepods

Abstract Ecological speciation, the formation of reproductive barriers as a consequence of adaptive divergence, can be a widespread diversification process in lacustrine landscapes, where the interplay of multiple biotic and abiotic factors generates a lavish array of divergent environments. Copepods are a major component of aquatic ecosystems and have remarkable evolvability, but the effects of adaptation to divergent environments at the genomic level and their implications for diversification in lakes are unknown. We studied four populations of calanoid copepods (Leptodiaptomus group sicilis) inhabiting three permanent deep lakes and one ephemeral playa lake; despite their geographical closeness, they display adaptation to local conditions of salinity, potential immigrant inviability and divergent life‐history traits. Using a reduced representation of the genome, we describe the genomic signatures of ecological divergence (salinity and habitat permanence), genome‐wide differentiation and population structure. We found that the four populations are genetically well‐differentiated and constitute four monophyletic lineages with individual evolutionary trajectories. Candidate adaptive loci showed clear signatures of diversifying selection, and the relationship between neutral and adaptive genetic variation suggested a pattern of isolation‐by‐adaptation. Interestingly, most neutral and adaptive differentiation was associated with habitat permanence, not with salinity divergence. We concluded that local adaptation to salinity promoted reduced gene flow via immigrant inviability, reinforcing the adaptation to other factors associated with the permanence/ephemerality of lakes and fostering the accumulation of genomic differentiation due to neutral evolution, ultimately leading to speciation. Our results show how divergent ecological conditions such as salinity and permanence/ephemerality of water regime produce significant genomic differentiation in copepod populations, paving the way for their diversification and speciation.

Predicting the occurrence of host‐associated differentiation in parasitic arthropods: a quantitative literature review

AbstractParasite populations associated with different host species can encounter a variety of isolating reproductive barriers, leading to each population independently accumulating genome‐wide genetic differences due to their host associations. This phenomenon is called host‐associated differentiation (HAD) and has been proposed as an indicator of early diversification among parasitic arthropods. Although many parasite–host case study systems have been tested for the genetic signature of HAD (e.g., FST≥0.15 between sympatric, host‐associated populations in the absence of allopatry), it is unknown which isolating reproductive barriers best predict the general occurrence of HAD. HAD development has been attributed to biological and ecological factors that either directly generate reproductive isolation between parasites living on different hosts, such as ‘immigrant inviability’ (i.e., lower fitness of immigrants in non‐native environments), or that promote the accumulation of host‐specific genetic adaptations, such as the gallmaking feeding mode. In fact, some of these factors are shared across multiple case studies, suggesting that the occurrence of HAD is generalizable and can be predicted based on the incidence of significant biological and ecological factors. By means of a discriminant function analysis (DFA), this research assessed 108 arthropod parasite–host case studies for ecological and biological factors significantly correlated with the occurrence of HAD and whether these factors could be used to distinguish the presence of HAD from its absence. The DFA demonstrated that case studies that developed HAD could be distinguished from case studies that did not develop HAD. The results of the DFA were corroborated by a ‘non‐iterative partial least squares’ (NIPALS) discriminant model and a nominal logistic regression. Case studies with HAD could be robustly separated from case studies without HAD based on the incidence of these predictive factors: immigrant inviability, gallmaking, endophagy, recent range invasions of either hosts or parasites, differential host phenology, and differential parasite morphology. These results were used in an infinite random forest analysis to generate a hierarchy of conditional probabilities that separated HAD presence from absence. The results provide researchers with a tool for reliably predicting which untested parasite–host system would likely develop HAD. Immigrant inviability, gallmaking, and their combination were strongly correlated with the presence of HAD, which indicated parasite–host systems with these traits were highly likely to develop HAD. Contrary to expectation, endophagous feeding was negatively correlated with HAD presence, which indicated phytophagous endophagous feeders (excepting gallmakers) were highly unlikely to develop HAD. Furthermore, parasitoids were shown to be just as likely to develop HAD as not. Unfortunately, potentially significant predictive factors (e.g., allochrony) were excluded from analysis because too few case studies have been specifically tested for these factors. Furthermore, this analysis was biased by the lack of ‘negative’ publication results and the overrepresentation of research laboratories that primarily study HAD. Future research should accumulate novel HAD case studies that specifically test for allochrony, differential microbial associations, and morphological differentiation.

Asymmetric, but opposing reductions in immigrant viability and fecundity promote reproductive isolation among host-associated populations of an insect herbivore.

Immigrant inviability can contribute to reproductive isolation (RI) during ecological speciation by reducing the survival of immigrants in non-native environments. However, studies that assess the fitness consequence of immigrants moving from native to non-native environments typically fail to explore the potential role of concomitant reductions in immigrant fecundity despite recent evidence suggesting its prominent role during local adaptation. Here, we evaluate the directionality and magnitude of both immigrant viability and fecundity to RI in a host-specific gall-forming wasp, Belonocnema treatae. Using reciprocal transplant experiments replicated across sites, we measure immigrant viability and fecundity by comparing differences in the incidence of gall formation (viability) and predicted the number of eggs per female (fecundity) between residents and immigrants in each of two host-plant environments. Reduced immigrant viability was found in one host environment while reduced immigrant fecundity was found in the other. Such habitat-dependent barriers resulted in asymmetric RI between populations. By surveying recent literature on local adaptation, we find that asymmetry in immigrant viability and fecundity are widespread across disparate taxa, which highlights the need to combine estimates of both common and overlooked barriers in cases of potential bi-directional gene flow to create a more comprehensive view of the evolution of RI.

Varieties of the highly dispersible and hypervariable tree, Metrosideros polymorpha, differ in response to mechanical stress and light across a sharp ecotone.

The drivers of isolation between sympatric populations of long-lived and highly dispersible conspecific plants are not well understood. In the Hawaiian Islands, the landscape-dominant tree, Metrosideros polymorpha, displays extraordinary phenotypic differences among sympatric varieties despite high dispersibility of its pollen and seeds, thereby presenting a unique opportunity to investigate how disruptive selection alone can maintain incipient forms. Stenophyllous M. polymorpha var. newellii is a recently evolved tree endemic to the waterways of eastern Hawai'i Island that shows striking neutral genetic differentiation from its ancestor, wet-forest M. polymorpha var. glaberrima, despite sympatry of these forms. We looked for evidence for, and drivers of, differential local adaptation of these varieties across the range of M. polymorpha var. newellii. For paired populations of these varieties, we compared seedling performance under contrasting light conditions and a strong water current characteristic of the riparian zone. We also conducted a reciprocal transplant experiment and contrasted adult leaf anatomy. Results suggest that the riparian zone is harsh and that selection involving the mechanical stress of rushing water, and secondarily, light, led to significant reciprocal immigrant inviability in adjacent forest and riparian environments. The strongest adaptive divergence between varieties was seen in leaves and seedlings from the site with the sharpest ecotone, coincident with the strongest genetic isolation of M. polymorpha var. newellii observed previously. These findings suggest that disruptive selection across a sharp ecotone contributes to the maintenance of an incipient riparian ecotype from within a continuous population of a long-lived and highly dispersible tree species.

Immigrant and extrinsic hybrid inviability contribute to reproductive isolation between lake and river cichlid ecotypes.

Understanding how reproductive barriers evolve and which barriers contribute to speciation requires the examination of organismal lineages that are still in the process of diversification and the study of the full range of reproductive barriers acting at different life stages. Lake and river ecotypes of the East African cichlid fish Astatotilapia burtoni show habitat-specific adaptations, despite different levels of genetic differentiation, and thus represent an ideal model to study the evolution of reproductive barriers. To evaluate the degree of reproductive isolation between genetically divergent lake and river populations, we performed a mesocosm mating experiment in a semi-natural setting at Lake Tanganyika. We assessed reproductive isolation in the presence of male-male competition by analyzing survival and growth rates of introduced adults and their reproductive success from genetic parentage of surviving offspring. The genetically divergent river population showed reduced fitness in terms of survival, growth rate, and mating success in a lake-like environment. Hybrid offspring between different populations showed intermediate survival consistent with extrinsic postzygotic reproductive barriers. Our results suggest that both prezygotic (immigrant inviability) and postzygotic reproductive barriers contribute to divergence, and highlight the value of assessing multiple reproductive barriers acting at different stages and in natural contexts to understand speciation mechanisms.

Acclimatory capacity of the Gorgonian Isis hippuris Linnaeus, 1758 to environmental change in SE Sulawesi, Indonesia

Coral reefs within the Indonesian archipelago are some of the most biodiverse yet anthropogenically compromised marine ecosystems. Within the Wakatobi Marine National Park (WMNP), SE Sulawesi, Indonesia, pronounced environmental clines are either caused or exacerbated by marine resource subsistence and destruction. The protected zooxanthellate gorgonian (sea fan coral) Isis hippuris Linnaeus, 1758 however, thrives on degraded reefs, with distinct morphotypes across contrasting reef environments within the region. To investigate if I. hippuris morphotypes are environmentally induced (plastic) or genetically derived (fixed), reciprocal transplant experiments (RTEs) were conducted across environmental gradients of light attenuation and anthropogenic disturbance. Phenotypic traits were measured and grouped into modules (colony, polyps, sclerites, optical parameters) to assess the physiological responses and endosymbiont specificity of each I. hippuris morphotype to environmental change. Trait modules were then modelled for tests of integration to determine phenotypic traits that interact to delimit I. hippuris morphotypes in response to environmental perturbation. After one-year, survivorship was lowest in clones transplanted from healthy to the degraded reef, suggesting the onset of immigrant inviability. Multivariate analyses revealed that phenotypic traits in healthy source colonies consistently showed significant trait plasticity, whereas residents from the impacted site were relatively insensitive to environmental change. Of the 38 phenotypic traits assessed, 17 were identified as driving test dissimilarities, most notably in branching dynamics, polyp density, capstan and spindle sclerite dimensions, and Symbiodinium chlorophyll a light energy absorbance efficiency (for photosynthesis). Specifically, photoacclimatory responses were integrated at the morphological and bio-optical levels, with chlorophyll a light harvesting efficiency maintained during reduced pigment density resulting from an increase in host sclerite articulation that maximized the internal light field in healthy clones on degraded reefs. Variable optical responses were not attributed to endosymbiont type, as all test colonies possessed a novel Symbiodinium Clade D1a. In summary, patterns of phenotypic variability within the I. hippuris holobiont likely represent incipient ecological divergence, with a high capacity for plasticity that has become fixed through ongoing anthropogenic disturbance on degraded reefs.

Do assortative mating and immigrant inviability help maintain population genetic structuring of an herbivore on a crop and a wild relative?

Population genetic structuring is common among herbivorous insects and frequently is associated with divergent host plants, such as crops and their wild relatives. Previous studies showed population genetic structuring in corn leafhopper Dalbulus maidis in Mexico, such that the species consists of two sympatric, host plant-associated populations: an abundant and widespread "pestiferous" population on maize (Zea mays mays), and a small and localized "wild" population on perennial teosinte (Zea diploperennis), a maize wild relative with a limited distribution. This study addressed whether assortative mating and immigrant inviability mediate genetic structuring of corn leafhopper by comparing the mating and reproductive successes of pestiferous and wild females that colonize their nonassociated host plants against the successes of females colonizing their associated host plants. Assortative mating was assessed by comparing mating frequencies and premating and mating times among females of each population on each host plant; immigrant inviability was assessed by comparing, across two generations, the fecundity, survival, development time, sex ratio, and population growth rate among leafhopper populations and host plants. Our results showed that on maize, and compared to resident, pestiferous females, wild females were more likely to mate, and greater proportions of their offspring survived to adult stage and were daughters; consequently, the per-generation population growth rate on maize was greater for immigrant, wild leafhoppers compared to resident, pestiferous leafhoppers. Our results suggested that wild leafhoppers emigrating to maize have a fitness advantage over resident, pestiferous leafhoppers, while immigrant pestiferous and resident wild leafhoppers on teosinte have similar fitnesses.

Immigrant reproductive dysfunction facilitates ecological speciation.

The distributions of species are not only determined by where they can survive - they must also be able to reproduce. Although immigrant inviability is a well-established concept, the fact that immigrants also need to be able to effectively reproduce in foreign environments has not been fully appreciated in the study of adaptive divergence and speciation. Fertilization and reproduction are sensitive life-history stages that could be detrimentally affected for immigrants in non-native habitats. We propose that "immigrant reproductive dysfunction" is a hitherto overlooked aspect of reproductive isolation caused by natural selection on immigrants. This idea is supported by results from experiments on an externally fertilizing fish (sand goby, Pomatoschistus minutus). Growth and condition of adults were not affected by non-native salinity whereas males spawning as immigrants had lower sperm motility and hatching success than residents. We interpret these results as evidence for local adaptation or acclimation of sperm, and possibly also components of paternal care. The resulting loss in fitness, which we call "immigrant reproductive dysfunction," has the potential to reduce gene flow between populations with locally adapted reproduction, and it may play a role in species distributions and speciation.

Immigrant and extrinsic hybrid seed inviability contribute to reproductive isolation between forest and dune ecotypes of Epipactis helleborine (Orchidaceae)

Reproductive isolation caused by divergent natural selection arising from differences between ecological environments or ecological interactions represents a major mechanism contributing to speciation, but its relative importance is poorly known. In this study, controlled reciprocal crossings and seed germination experiments were combined with genetic and morphometric analyses to test the hypothesis that previously described differences in mycorrhizal communities between forest and dune ecotypes of Epipactis helleborine were sufficiently strong to create complete reproductive isolation between the two ecotypes. Molecular analyses using 770 SNP markers showed that the two ecotypes were genetically distinct and that populations of the dune ecotype were genetically impoverished compared to populations of the forest ecotype. Morphologically, the two ecotypes were also significantly different, with plants of the dune ecotype generally being smaller than plants of the forest ecotype. The results further showed that immigrant seeds had a significantly lower probability of protocorm formation than native seeds, indicating strong immigrant inviability. Although both ecotypes were able to cross easily and to produce a large number of viable seeds, hybrid seeds showed significantly lower protocorm formation than pure seeds, further contributing to reproductive isolation. Overall, these results indicate that interfertile populations of a widespread orchid adapting to contrasting environments diverge as a consequence of concurrent selection acting against immigrants and hybrids and suggest that mycorrhizal fungi can play a role in the early stages of plant speciation.

Assessing the Potential Contributions of Reduced Immigrant Viability and Fecundity to Reproductive Isolation.

Reduced fitness of immigrants from alternative environments is thought to be an important reproductive isolating barrier. Most studies evaluating the importance of the relative fitness of immigrants to speciation have focused on reduced survival of immigrants (i.e., immigrant inviability). However, variation in fecundity appears to have a greater impact on variation in fitness than does variation in viability, suggesting that reduced fecundity of immigrants could act as an important yet largely overlooked reproductive isolating barrier. Using a model and a survey of studies of local adaptation, we evaluate the relative strength of reduced immigrant viability and fecundity as potential causes of reproductive isolation. We found that reduced fecundity as compared to reduced viability as a reproductive isolating barrier should increase in importance as the relative costs of reproduction increase. Consistent with the elevated demands of reproduction reported in the literature, we found that reproductive isolation from reduced immigrant fecundity was of similar magnitude or greater than that from reduced immigrant viability, particularly in the early stages of speciation. These results suggest that the important role of differential fecundity in local adaptation extends to speciation.

Immigrant inviability promotes reproductive isolation among host‐associated populations of the gall wasp Belonocnema treatae

AbstractEcological speciation describes the evolutionary process whereby divergent natural selection between environments generates reproductive isolation. Studying the magnitude of sequential reproductive barriers between ecologically divergent populations improves our understanding of the way these barriers evolve and how each contributes to the speciation process. Immigrant inviability describes the lower fitness of immigrants in non‐native environments and is an important, but long underexplored, reproductive barrier. In this study, we test the role of immigrant inviability among host‐associated populations of the gall wasp Belonocnema treataeMayr (Hymenoptera: Cynipini: Cynipidae) by measuring the ability of gall wasps to initiate and complete gall formation, while avoiding host immune responses, on closely related native and non‐native live oaks, Quercus virginianaMill., Quercus fusiformisSmall, and Quercus geminataSmall (Fagaceae). In general, we found evidence for immigrant inviability when B. treatae populations colonized non‐native host species. However, patterns were variable among years, suggesting that episodic events may play an important role in connecting ecologically divergent populations.

Divergent natural selection promotes immigrant inviability at early and late stages of evolutionary divergence.

Natural selection's role in speciation has been of fundamental importance since Darwin first outlined his theory. Recently, work has focused on understanding how selection drives trait divergence, and subsequently reproductive isolation. "Immigrant inviability," a barrier that arises from selection against immigrants in their nonnative environment, appears to be of particular importance. Although immigrant inviability is likely ubiquitous, we know relatively little about how selection acts on traits to drive immigrant inviability, and how important immigrant inviability is at early-versus-late stages of divergence. We present a study evaluating the role of predation in the evolution of immigrant inviability in recently diverged population pairs and a well-established species pair of Brachyrhaphis fishes. We evaluate performance in a high-predation environment by assessing survival in the presence of a predator, and swimming endurance in a low-predation environment. We find strong signatures of local adaptation and immigrant inviability of roughly the same magnitude both early and late in divergence. We find remarkably conserved selection for burst-speed swimming (important in predator evasion), and selection for increased size in low-predation environments. Our results highlight the consistency with which selection acts during speciation, and suggest that similar factors might promote initial population differentiation and maintain differentiation at late stages of divergence.

From local adaptation to ecological speciation in copepod populations from neighboring lakes.

Continental copepods have been derived from several independent invasive events from the sea, but the subsequent evolutionary processes that account for the current diversity in lacustrine environments are virtually unknown. Salinity is highly variable among lakes and constitutes a source of divergent selection driving potential reproductive isolation. We studied four populations of the calanoid copepod Leptodiaptomus cf. sicilis inhabiting four neighboring lakes with a common history (since the Late Pleistocene) located in the Oriental Basin, Mexico; one lake is shallow and varies in salinity periodically (1.4–10 g L-1), while three are deep and permanent, with constant salinity (0.5, 1.1 and 6.5 g L-1, respectively). We hypothesized that (1) these populations belong to a different species than L. sicilis sensu stricto and (2) are experiencing ecologically based divergence due to salinity differences. We assessed morphological and molecular (mtDNA) COI variation, as well as fitness differences and tests of reproductive isolation. Although relationships of the Mexican populations with L. sicilis s.s. could not be elucidated, we identified a clear pattern of divergent selection driven by salinity conditions. The four populations can still be considered a single biological species (sexual recognition and hybridization are still possible in laboratory conditions), but they have diverged into at least three different phenotypes: two locally adapted, specialized in the lakes of constant salinity (saline vs. freshwater), and an intermediate generalist phenotype inhabiting the temporary lake with fluctuating salinity. The specialized phenotypes are poorly suited as migrants, so prezygotic isolation due to immigrant inviability is highly probable. This implication was supported by molecular evidence that showed restricted gene flow, persistence of founder events, and a pattern of allopatric fragmentation. This study showed how ecologically based divergent selection may explain diversification patterns in lacustrine copepods.

Batesian mimicry promotes pre- and postmating isolation in a snake mimicry complex.

We evaluated whether Batesian mimicry promotes early-stage reproductive isolation. Many Batesian mimics occur not only in sympatry with their model (as expected), but also in allopatry. As a consequence of local adaptation within both sympatry (where mimetic traits are favored) and allopatry (where nonmimetic traits are favored), divergent, predator-mediated natural selection should disfavor immigrants between these selective environments as well as any between-environment hybrids. This selection might form the basis for both pre- and postmating isolation, respectively. We tested for such selection in a snake mimicry complex by placing clay replicas of sympatric, allopatric, or hybrid phenotypes in both sympatry and allopatry and measuring predation attempts. As predicted, replicas with immigrant phenotypes were disfavored in both selective environments. Replicas with hybrid phenotypes were also disfavored, but only in a region of sympatry where previous studies have detected strong selection favoring precise mimicry. By fostering immigrant inviability and ecologically dependent selection against hybrids (at least in some habitats), Batesian mimicry might therefore promote reproductive isolation. Thus, although Batesian mimicry has long been viewed as a mechanism for convergent evolution, it might play an underappreciated role in fueling divergent evolution and possibly even the evolution of reproductive isolation and speciation.

Strong natural selection on juveniles maintains a narrow adult hybrid zone in a broadcast spawner.

Natural selection can maintain and help form species across different habitats, even when dispersal is high. Selection against inferior migrants (immigrant inviability) acts when locally adapted populations suffer high mortality on dispersal to unsuitable habitats. Habitat-specific populations undergoing divergent selection via immigrant inviability should thus show (1) a change in the ratio of adapted to nonadapted individuals among age/size classes and (2) a cline (defined by the environmental gradient) as selection counterbalances migration. Here we examine the frequencies of two depth-segregated lineages in juveniles and adults of a Caribbean octocoral, Eunicea flexuosa. Distributions of the two lineages in both shallow and deep environments were more distinct when inferred from adults than juveniles. Despite broad larval dispersal, we also found an extremely narrow hybrid zone (<100 m), with coincident clines for molecular and morphological characters of the host coral and its algal symbiont. Effective dispersal estimates derived from the hybrid zone are remarkably small (<20 m) for a broadcast spawner. The large selection coefficient against mismatched genotypes derived from cohort data is consistent with that from field transplant experiments. Narrow hybrid zones and limited effective dispersal may be a common outcome of long periods of postsettlement, prereproductive selection across steep ecological gradients. Strong diversifying selection provides a mechanism to explain the prevalence of depth-segregated sibling species in the sea.

Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral

Long-lived corals, the foundation of modern reefs, often follow ecological gradients, so that populations or sister species segregate by habitat. Adaptive divergence maintains sympatric congeners after secondary contact or may even generate species by natural selection in the face of gene flow. Such ecological divergence, initially between alternative phenotypes within populations, may be aided by immigrant inviability, especially when a long period separates larval dispersal and the onset of reproduction, during which selection can sort lineages to match different habitats. Here, we evaluate the strength of one ecological factor (depth) to isolate populations by comparing the genes and morphologies of pairs of depth-segregated populations of the candelabrum coral Eunicea flexuosa across the Caribbean. Eunicea is endemic to the Caribbean and all sister species co-occur. Eunicea flexuosa is widespread both geographically and across reef habitats. Our genetic analysis revealed two depth-segregated lineages. Field survivorship data, combined with estimates of selection coefficients based on transplant experiments, suggest that selection is strong enough to segregate these two lineages. Genetic exchange between the Shallow and Deep lineages occurred either immediately after divergence or the two have diverged with gene flow. Migration occurs asymmetrically from the Shallow to Deep lineage. Limited recruitment to reproductive age, even under weak annual selection advantage, is sufficient to generate habitat segregation because of the cumulative prolonged prereproductive selection. Ecological factors associated with depth can act as filters generating strong barriers to gene flow, altering morphologies, and contributing to the potential for speciation in the sea.

Host‐jump drives rapid and recent ecological speciation of the emergent fungal pathogen Colletotrichum kahawae

Ecological speciation through host-shift has been proposed as a major route for the appearance of novel fungal pathogens. The growing awareness of their negative impact on global economies and public health created an enormous interest in identifying the factors that are most likely to promote their emergence in nature. In this work, a combination of pathological, molecular and geographical data was used to investigate the recent emergence of the fungus Colletotrichum kahawae. C. kahawae emerged as a specialist pathogen causing coffee berry disease in Coffea arabica, owing to its unparalleled adaptation of infecting green coffee berries. Contrary to current hypotheses, our results suggest that a recent host-jump underlay the speciation of C. kahawae from a generalist group of fungi seemingly harmless to coffee berries. We posit that immigrant inviability and a predominantly asexual behaviour could have been instrumental in driving speciation by creating pleiotropic interactions between local adaptation and reproductive patterns. Moreover, we estimate that C. kahawae began its diversification at <2200 bp leaving a very short time frame since the divergence from its sibling lineage (c. 5600 bp), during which a severe drop in C. kahawae's effective population size occurred. This further supports a scenario of recent introduction and subsequent adaptation to C. arabica. Phylogeographical data revealed low levels of genetic polymorphism but provided the first geographically consistent population structure of C. kahawae, inferring the Angolan population as the most ancestral and the East African populations as the most recently derived. Altogether, these results highlight the significant role of host specialization and asexuality in the emergence of fungal pathogens through ecological speciation.

Immigrant inviability in yellow pecan aphid

1. Host-associated differentiation (HAD) may be an important driver of parasite biodiversity. The sympatric occurrence of host-associated populations features prominently in studies documenting HAD but this neither confirms nor denies that the lineages arose in sympatry. It does raise the question of what maintains such structure despite the proximity of populations in space and time. 2. We tested for immigrant inviability in yellow pecan aphid Monelliopsis pecanis Bissell, a species previously shown to be host associated, using a laboratory reciprocal transplant experiment on pecan and water hickory. 3. Immigrant inviability on the alternative host is present in yellow pecan aphid. Immigrants to both hosts were significantly less fecund than residents and their nymphs were significantly less viable. Future studies should establish the genetic and non-genetic (maternal effects) basis of immigrant inviability in yellow pecan aphid in order to be certain about its contribution to pre-mating reproductive isolation. 4. Since aphids are cyclic parthenogens, inviability of both immigrants and their offspring has the potential to contribute to total pre-mating reproductive isolation. This is different than the case of obligate sexually reproducing organisms where offspring viability is a post-mating reproductive isolating mechanism. We discuss the implications of this for estimating the contributions of immigrant and offspring inviability to total reproductive isolation in aphids.

Divergent host plant specialization as the critical driving force in speciation between populations of a phytophagous ladybird beetle

Detecting the isolating barrier that arises earliest in speciation is critically important to understanding the mechanism of species formation. We tested isolating barriers between host races of a phytophagous ladybird beetle, Henosepilachna diekei (Coleoptera: Coccinellidae: Epilachnine), that occur sympatrically on distinct host plants. We conducted field surveys for the distribution of the beetles and host plants, rearing experiments to measure six potential isolating factors (adult host preference, adult and larval host performance, sexual isolation, egg hatchability, F(1) hybrid inviability, and sexual selection against F(1) hybrids), and molecular analyses of mitochondrial ND2 and the nuclear ITS2 sequences. We found significant genetic divergence between the host races, and extremely divergent host preference (i.e. habitat isolation) and host performance (i.e. immigrant inviability), but no other isolating barriers. The fidelity to particular host plants arises first and alone can prevent gene flow between differentiating populations of phytophagous specialists.