CASE STUDIES AND MATHEMATICAL MODELS OF ECOLOGICAL SPECIATION. 4. HYBRID SPECIATION IN BUTTERFLIES IN A JUNGLE

We build a spatial individual-based multilocus model of homoploid hybrid speciation tailored for a tentative case of hybrid origin of Heliconius heurippa from H. melpomene and H. cydno in South America. Our model attempts to account for empirical patterns and data on genetic incompatibility, mating preferences and selection by predation (both based on coloration patterns), habitat preference, and local adaptation for all three Heliconius species. Using this model, we study the likelihood of recombinational speciation and identify the effects of various ecological and genetic parameters on the dynamics, patterns, and consequences of hybrid ecological speciation. Overall, our model supports the possibility of hybrid origin of H. heurippa under certain conditions. The most plausible scenario would include hybridization between H. melpomene and H. cydno in an area geographically isolated from the rest of both parental species with subsequent long-lasting geographic isolation of the new hybrid species, followed by changes in the species ranges, the secondary contact, and disappearance of H. melpomene -type ecomorph in the hybrid species. However, much more work (both empirical and theoretical) is necessary to be able to make more definite conclusions on the importance of homoploid hybrid speciation in animals.     

ECOLOGICAL SPECIATION IN STICKLEBACKS: ENVIRONMENT-DEPENDENT HYBRID FITNESS

“Ecological” speciation occurs when reproductive isolation evolves as a consequence of divergent selection between populations exploiting different resources or environments. We tested this hypothesis of speciation in a young stickleback species pair by measuring the direct contribution of ecological selection pressures to hybrid fitness. The two species (limnetic and benthic) are strongly differentiated morphologically and ecologically, whereas hybrids are intermediate. Fitness of hybrids is high in the laboratory, especially F₁ and F₂ hybrids (backcrosses may show some breakdown). We transplanted F₁ hybrids to enclosures in the two main habitats in the wild to test whether the distribution of resources available in the environment generates a hybrid disadvantage not detectable in the laboratory. Hybrids grew more slowly than limnetics in the open water habitat and more slowly than benthics in the littoral zone. Growth of F₁ hybrids was inferior to the average of the parent species across both habitats, albeit not significantly. The contrast between laboratory and field results supports the hypothesis that mechanisms of F₁ hybrid fitness in the wild are primarily ecological and do not result from intrinsic genetic incompatibilities. Direct selection on hybrids contributes to the maintenance of sympatric stickleback species and may have played an important role in their origin.     

SPECIATION DUE TO HYBRID NECROSIS IN PLANT–PATHOGEN MODELS

We develop a model for speciation due to postzygotic incompatibility generated by autoimmune reactions. The model is based on frequency‐dependent interactions between host plants and their pathogens, which can generate disruptive selection and give rise to speciation if distant phenotypes become reproductively isolated. Based on recent experimental evidence from Arabidopsis, we assume that at the molecular level, incompatibility between host strains is caused by epistatic interactions between two proteins in the plant immune system—the guard and the guardee. Within each plant strain, immune reactions occur when the guardee protein is modified by a pathogen effector, and the guard subsequently binds to the guardee, thus precipitating an immune response. When guard and guardee proteins come from phenotypically distant parents, a hybrid's immune system can be triggered by erroneous interactions between these proteins even in the absence of pathogen attack, leading to severe autoimmune reactions in hybrids. This generates a Dobzhnasky–Muller incompatibility due to immune reactions. Our model shows how phenotypic variation generated by frequency‐dependent host–pathogen interactions can lead to such postzygotic incompatibilities between extremal types, and hence to speciation.     

TROPICS ACCELERATE THE EVOLUTION OF HYBRID MALE STERILITY IN DROSOPHILA

Understanding the evolutionary mechanisms that facilitate speciation and explain global patterns of species diversity has remained a challenge for decades. The most general pattern of species biodiversity is the latitudinal gradient, whereby species richness increases toward the tropics. Although such a global pattern probably has a multitude of causes, recent attention has focused on the hypothesis that speciation and the evolution of reproductive isolation occur faster in the tropics. Here, I tested this prediction using a dataset on premating and postzygotic isolation between recently diverged Drosophila species. Results showed that while the evolution of premating isolation was not greater between tropical Drosophila relative to nontropical species, postzygotic isolation evolved faster in the tropics. In particular, hybrid male sterility was much greater among tropical Drosophila compared to nontropical species pairs of similar genetic age. Several testable explanations for the novel pattern are discussed, including greater role for sterility‐inducing bacterial endosymbionts in the tropics and more intense sperm–sperm competition or sperm–egg sexual conflict in the tropics. The results imply that processes of speciation in the tropics may evolve at different rates or may even be somewhat different from those at higher latitudes.     

鸟类鸣声行为对其物种分化和新种形成影响

鸟声和鸟类的形态特征一样,具有物种的特异性,在鸟类分类和野外识别方面是有意义的,从生物种的基本概念出发,新种的形成有赖于两个亲缘种群间不能相互婚配和繁殖隔离的产生。鸟类主要的有关特征是在配对形成过程中的听觉和视觉特征,如果出现鸣声特征的差异,而且这种差异已经超出了种间“语言通讯”的变化范围,那么它就有可能与群内其它异笥无法配对,从而被排除到该种群或种的范围之外,然而鸣禽的鸣唱有时在不同种群间变化很大,而在同一种群内比较稳定,从而形成种群的方言,在方言种群之间,如果长期隔离,就会在种群之间形成障碍乃至遗传上的隔离,从而使种群间失去了相互配偶的机会,新的亚种或种可能由此形成,文章最后假设出了基于鸣声行为的鸟类新种形成机理图解。     

GENETIC STRUCTURE AND EVOLUTION OF A FIRE ANT HYBRID ZONE

Two introduced fire ants, Solenopsis invicta and S. richteri, hybridize over an extensive area in the United States spanning central Mississippi, Alabama, and western Georgia. We studied a portion of this hybrid zone in northwestern Mississippi in detail by sampling ants at many sites along two transects extending across the zone and examining gene frequency and size distributions at a large number of genetic and morphological markers. The distributional patterns at these markers are most consistent with the mosaic hybrid zone model, whereby the distribution of various fire ant genotypes is determined initially by the historical patterns of colonization of newly available habitats. However, these distributional patterns probably do not reflect the equilibrium state of interactions because of the very recent secondary contact of the species (< 60 yr) and the dynamic nature of available nesting habitats in this area. Our data suggest that, with prolonged contact and interaction, differential fitness of various hybrid genotypes due to intrinsic and extrinsic selective factors is important in structuring the hybrid zone. For instance, consistent differential introgression of morphological and genetic markers, combined with previous evidence of differences in developmental stability among genotypes, suggest reduced fitness of hybrids relative to parentals due to intrinsic selection (as may be caused by breakup of parental gene complexes). Furthermore, marked reductions in the occurrence of parental-like hybrids in areas where the similar parental species is common suggest reduced fitness of these parental-like hybrids in competition with the parentals (i.e., extrinsic selection). Because the relative roles of such deterministic as well as stochastic forces apparently vary both spatially and temporally, the eventual distribution of the various fire ant genotypes and the fate of the hybrid zone in the United States is difficult to predict.     

FINE-SCALE GENETIC AND PHENOTYPIC STRUCTURE IN NATURAL POPULATIONS OF BACILLUS SUBTILIS AND BACILLUS LICHENIFORMIS: IMPLICATIONS FOR BACTERIAL EVOLUTION AND SPECIATION

The genetic and phenotypic structure of sympatric populations of wild bacteria traditionally identified as Bacillus subtilis and B. licheniformis was analyzed. Small soil samples were taken from a single, tiny site in the Sonoran Desert of Arizona, USA, to provide a true population analysis, in contrast to many analyses of genetic structure using bacterial strain collections of widely heterogeneous origin. Genetic analyses of isolates used multilocus enzyme electrophoresis, mismatches in restriction fragment length polymorphism, and variants from Southern hybridization with B. subtilis DNA probes. Phenotypic analyses of isolates used the API test system for detection of growth and acid production on specific carbon sources. The two species were distinct both phenotypically and genetically, despite their known potential for genetic exchange in laboratory experiments. Genic and genotypic diversity were high in both species, and only 16% of observed allozyme variants might possibly be common to both species. Hence, there is probably modest genetic exchange, if any, between the species in nature. Clear hierarchies of population-genetic structure were found for both species. Different types of genetic data yield concordant population structures for B. subtilis. For both species, two-locus and multilocus statistical analyses of linkage demonstrated modest to strong disequilibrium at the species level but truly panmictic subunits within each species. The evidence for extensive genetic recombination within these fine-scale subdivisions is unequivocal, indicating that the sexuality of these bacteria can be well expressed in nature. The relation of these results to processes of bacterial evolution and speciation is discussed.     

THE DIVERSITY AND EVOLUTION OF BATESIAN MIMICRY IN PAPILIO SWALLOWTAIL BUTTERFLIES

Papilio swallowtail butterflies exhibit a remarkable diversity of Batesian mimicry, manifested in several sex-limited and polymorphic types. There is little understanding of how this diversity is distributed within Papilio , and how different mimicry types have evolved in relation to each other. To answer these questions, I present a graphical model that connects various mimicry types by hypothetical character state changes within a phylogenetic framework. A maximum likelihood analysis of evolution of mimicry types on the Papilio phylogeny showed that sexually monomorphic mimicry and female-limited mimicry have evolved repeatedly but predominantly independently in different clades. However, transitions between these mimicry types are rarely observed. The frequency distribution of character state changes was skewed in favor of the evolution of mimicry, whereas many theoretically plausible character state changes, especially evolutionary loss of mimicry, were not evident. I discuss these findings in relation to studying the tempo of evolutionary change, loss of traits, and directionality and connectivity among character states. The pathway approach and phylogenetic patterns of mimicry demonstrated in Papilio are useful to test novel hypotheses regarding the diversity and evolutionary directionality of Batesian mimicry in other systems.     

LIFE-HISTORY ADAPTATION AND REPRODUCTIVE ISOLATION IN A GRASSHOPPER HYBRID ZONE

Patterns of life-history adaptation and reproductive isolation were investigated in the acridid grasshoppers Melanoplus sanguinipes and M. devastator, which hybridize along an altitudinal gradient in the Sierra Nevada of California. Melanoplus sanguinipes females crossed with M. devastator males produced eggs that were approximately half as viable as eggs from other crosses. Diminished viability was not attributable either to infection by Wolbachia pipientis or to failure of sperm transfer. When offered an opportunity to choose a mate, females from all populations discriminated against males of the other species, whereas in no-choice tests measuring copulation duration only females from the tails of the clines showed preferences. Melanoplus sanguinipes, found at high elevations where the growing season is short, exhibited faster egg hatch, faster larval development, smaller adult body sizes, and smaller clutch sizes than M. devastator. Melanoplus devastator, from California's Central Valley, endured a hot and dry summer in a reproductive diapause that was absent in M. sanguinipes. Clines in reproductive diapause and clutch size coincided with the region of reproductive incompatibility. Development time, body size, and hatch time also changed across the hybrid zone, but the regions of largest transitions in these traits were either difficult to locate using the limited populations studied here or were not coincident with the zone's center. A method is described for combining ecological and phylogenetic analyses to address the unknown issue of whether life-history divergence has conributed to reproductive isolation in this system.     

FEMALE HETEROGAMETY AND SPECIATION: REDUCED INTROGRESSION OF THE Z CHROMOSOME BETWEEN TWO SPECIES OF NIGHTINGALES

Several lines of evidence suggest that the X chromosome plays a large role in intrinsic postzygotic isolation. The role of the Z chromosome in speciation is much less understood. To explore the role of the Z chromosome in reproductive isolation, we studied nucleotide variation in two closely related bird species, the Thrush Nightingale ( Luscinia luscinia ) and the Common Nightingale ( L. megarhynchos ). These species are isolated by incomplete prezygotic isolation and female hybrid sterility. We sequenced introns of four Z-linked and eight autosomal loci and analyzed patterns of polymorphism and divergence using a divergence-with-gene flow framework. Our results suggest that the nightingale species diverged approximately 1.8 Mya. We found strong evidence of gene flow after divergence in both directions, although more introgression occurred from L. megarhynchos into L. luscinia . Gene flow was significantly higher on the autosomes than on the Z chromosome. Our results support the idea that the Z chromosome plays an important role in intrinsic postzygotic isolation in birds, although it may also contribute to the evolution of prezygotic isolation through sexual selection. This highlights the similarities in the genetic basis of reproductive isolation between organisms with heterogametic males and organisms with heterogametic females during the early stages of speciation.     

ORIGINS,EVOLUTION, AND DIVERSIFICATION OF CLEPTOPARASITIC LINEAGES IN LONG‐TONGUED BEES

The evolution of parasitic behavior may catalyze the exploitation of new ecological niches yet also binds the fate of a parasite to that of its host. It is thus not clear whether evolutionary transitions from free‐living organism to parasite lead to increased or decreased rates of diversification. We explore the evolution of brood parasitism in long‐tongued bees and find decreased rates of diversification in eight of 10 brood parasitic clades. We propose a pathway for the evolution of brood parasitic strategy and find that a strategy in which a closed host nest cell is parasitized and the host offspring is killed by the adult parasite represents an obligate first step in the appearance of a brood parasitic lineage; this ultimately evolves into a strategy in which an open host cell is parasitized and the host offspring is killed by a specialized larval instar. The transition to parasitizing open nest cells expanded the range of potential hosts for brood parasitic bees and played a fundamental role in the patterns of diversification seen in brood parasitic clades. We address the prevalence of brood parasitic lineages in certain families of bees and examine the evolution of brood parasitism in other groups of organisms.     

MULTIPLE MODES OF SPECIATION INVOLVED IN THE PARALLEL EVOLUTION OF SYMPATRIC MORPHOTYPES OF LAKE WHITEFISH (COREGONUS CLUPEAFORMIS,SALMONIDAE)

We performed a phylogenetic analysis of mtDNA variation among seven sympatric pairs of dwarf and normal morphotypes of whitefish from northern Québec and the St. John River drainage to address three questions relevant to understanding their radiation. Are all sympatric pairs reproductively isolated? Do phylogenetic analyses confirm that sympatric whitefish morphotypes found in eastern North America represent the outcome of polyphyletic evolutionary events? If so, did all sympatric pairs from the St. John River drainage originate from the same scenario of allopatric divergence and secondary contact? The hypothesis of genetic differentiation was supported for all sympatric pairs from the St. John River drainage, whereas lack of mtDNA diversity precluded any test of reproductive isolation for northern Québec populations. Patterns of mtDNA variation confirmed that dwarf and normal morphotypes evolved in parallel among independent, yet closely related, lineages, thus providing indirect evidence for the role of natural selection in promoting phenotypic radiation in whitefish. Patterns of mtDNA diversity among sympatric pairs of the St. John River indicated a complex picture of whitefish evolution that implied sympatric divergence and multiple allopatric divergence/secondary contact events on a small geographic scale. These results suggests that ecological opportunities, namely trophic niche availability, may promote population divergence in whitefish.     

THE ANIMAL WITHIN: CARCINOGENESIS AND THE CLONAL EVOLUTION OF CANCER CELLS ARE SPECIATION EVENTS SENSU STRICTO

Heritable genomic variation and natural selection have long been acknowledged as striking parallels between evolution and cancer. The logical conclusion, that cancer really is a form of speciation, has seldom been expounded directly. My purpose is to reexamine the “cancer as species” thesis in the light of current attitudes to asexual speciation, and modern analyses of species definitions. The chief obstacles to accepting this thesis have been the asexual nature of cancer cell reproduction, the instability of the malignant genotype and phenotype, and our conditioning that speciation is an extremely rare and imperceptibly gradualistic process. However, these are not absolute barriers to the acceptance of cancers as bona fide species. Furthermore, although ongoing clonal evolution of extant cancers also results in a series of secondary speciation events, the initial emergence of a cancer requires a level of taxonomic reclassification even beyond the concept of speciation (i.e., phylogenation), and which is almost certain to provide a rich source of novel drug targets. The implications of the “cancer as species” idea may be as important for biology as for oncology, providing as it does an endless supply of observable if accelerated examples of a phenomenon once regarded as rare. From the perspective of cancer treatment, speciation guarantees the existence of causal molecular mechanisms which may have been neglected as exploitable targets for rational therapy; in particular, the mediators of metazoan life seem to have substantial overlap with components commonly deranged in cancer cells. However, the intractability of the drug resistance problem, residing as it does in the inherent plasticity of the genome, is traceable back to, and inseparable from, the very origins and nature of life.     

DYNAMICS OF HYBRID INCOMPATIBILITY IN GENE NETWORKS IN A CONSTANT ENVIRONMENT

After an ancestral population splits into two allopatric populations, different mutations may fix in each. When pairs of mutations are brought together in a hybrid offspring, epistasis may cause reduced fitness. Such pairs are known as Bateson–Dobzhansky–Muller (BDM) incompatibilities. A well-known model of BDM incompatibility due to Orr suggests that the fitness load on hybrids should initially accelerate, and continue to increase as the number of potentially incompatible substitutions increases (the "snowball effect"). In the gene networks model, which violates a key assumption of Orr's model (independence of fixation probabilities), the snowball effect often does not occur. Instead, we describe three possible dynamics in a constant environment: (1) Stabilizing selection can constrain two allopatric populations to remain near-perfectly compatible. (2) Despite constancy of environment, punctuated evolution may obtain; populations may experience rare adaptations asynchronously, permitting incompatibility. (3) Despite stabilizing selection, developmental system drift may permit genetic change, allowing two populations to drift in and out of compatibility. We reinterpret Orr's model in terms of genetic distance. We extend Orr's model to the finite loci case, which can limit incompatibility. Finally, we suggest that neutral evolution of gene regulation in nature, to the point of speciation, is a distinct possibility.     

GENETIC ARCHITECTURE AND POSTZYGOTIC REPRODUCTIVE ISOLATION: EVOLUTION OF BATESON–DOBZHANSKY–MULLER INCOMPATIBILITIES IN A POLYGENIC MODEL

The Bateson–Dobzhansky–Muller model predicts that postzygotic isolation evolves due to the accumulation of incompatible epistatic interactions, but few studies have quantified the relationship between genetic architecture and patterns of reproductive divergence. We examined how the direction and magnitude of epistatic interactions in a polygenic trait under stabilizing selection influenced the evolution of hybrid incompatibilities. We found that populations evolving independently under stabilizing selection experienced suites of compensatory allelic changes that resulted in genetic divergence between populations despite the maintenance of a stable, high‐fitness phenotype. A small number of loci were then incompatible with multiple alleles in the genetic background of the hybrid and the identity of these incompatibility loci changed over the evolution of the populations. For F₁ hybrids, reduced fitness evolved in a window of intermediate strengths of epistatic interactions, but F₂ and backcross hybrids evolved reduced fitness across weak and moderate strengths of epistasis due to segregation variance. Strong epistatic interactions constrained the allelic divergence of parental populations and prevented the development of reproductive isolation. Because many traits with varying genetic architectures must be under stabilizing selection, our results indicate that polygenetic drift is a plausible hypothesis for the evolution of postzygotic reproductive isolation.     

WEAK CROSSABILITY BARRIER BUT STRONG JUVENILE SELECTION SUPPORTS ECOLOGICAL SPECIATION OF THE HYBRID PINE PINUS DENSATA ON THE TIBETAN PLATEAU

Determining how a new hybrid lineage can achieve reproductive isolation is a key to understanding the process and mechanisms of homoploid hybrid speciation. Here, we evaluated the degree and nature of reproductive isolation between the ecologically successful hybrid species Pinus densata and its parental species P. tabuliformis and P. yunnanensis. We performed interspecific crosses among the three species to assess their crossability. We then conducted reciprocal transplantation experiments to evaluate their fitness differentiation, and to examine how natural populations representing different directions of introgression differ in adaptation. The crossing experiments revealed weak genetic barriers among the species. The transplantation trials showed manifest evidence of local adaptation as the three species all performed best in their native habitats. Pinus densata populations from the western edge of its distribution have evolved a strong local adaptation to the specific habitat in that range; populations representing different directions of introgressants with the two parental species all showed fitness disadvantages in this P. densata habitat. These observations illustrate that premating isolation through selection against immigrants from other habitat types or postzygotic isolation through selection against backcrosses between the three species is strong. Thus, ecological selection in combination with endogenous components and geographic isolation has likely played a significant role in the speciation of P. densata.     

THE GENETIC ARCHITECTURE OF REPRODUCTIVE ISOLATION IN LOUISIANA IRISES: HYBRID FITNESS IN NATURE

Negative epistasis in hybrid genomes commonly results in postzygotic isolation between divergent lineages. However, some genomic regions may be selectively neutral or adaptive in hybrids and thus may potentially cross species barriers. We examined postzygotic isolation between ecologically similar species of Louisiana Iris: Iris brevicaulis and I. fulva to determine the potential for adaptive introgression in nature. Line-cross analyses allowed us a general overview of the gene action responsible for fitness-related traits. We then used a QTL mapping approach to detect genomic regions responsible for variation in these traits. Although hybrid classes suffered reduced fitness for many traits, hybrid means were equivalent to at least one of the parental species in overall estimates of maternal and paternal fitness during the two years of the field study. The genetic architecture underlying the fitness-related traits varied across field site and year of the study, thus emphasizing the importance of the environment in determining the degree of postzygotic isolation and potential for introgression across natural hybrid zones.     

HYBRID ZONES AND HOST-PARASITE RELATIONSHIPS: EFFECT ON THE EVOLUTION OF PARASITIC SPECIFICITY

In southern France, Diplozoon gracile (Monogenea, Polyopisthocotylea), parasitizes four sympatric cyprinids. One of these host species, Barbus meridionalis, naturally hybridizes with another species of barbel, Barbus barbus, which is never parasitized by D. gracile under natural conditions. This hybridization has previously been studied and described as an introgression of B. barbus by B. meridionalis. The hybrids are parasitized by D. gracile, and parasite prevalence increases in proportion to the introgression rate, i.e., the percentage of B. meridionalis genes. The causes for this preferential distribution of the parasite in the hybrid population are analysed on the basis of ecological and ethological differences between the two parent species.