A gradient of pollination specialization in three species of Bolivian Centropogon.

PREMISE: Closely related plant species with overlapping ranges often experience competition for pollination services. Such competition can select for divergence in floral traits that attract pollinators or determine pollen placement. While most species in Centropogon (Campanulaceae: Lobelioideae) have flowers that suggest adaptation to bat or hummingbird pollination, actual pollinators are rarely documented, and a few species have a mix of traits from both pollination syndromes. We studied the pollination biology of a "mixed-syndrome" species and its co-occurring congeners to examine the relationship between floral traits and visitation patterns for Centropogon. METHODS: Fieldwork at two sites in Bolivian cloud forests involved filming floral visitors, quantifying pollen transfer, and measuring floral traits. Stamen exsertion, which determines pollen placement, was measured from herbarium specimens across the geographic range of these species to test for character displacement. RESULTS: Results show a generalization gradient, from primarily bat pollination in white-flowered Centropogon incanus, to bat pollination with secondary hummingbird pollination in the cream-flowered C. brittonianus, to equal reliance on both pollinators in the red-flowered, mixed-syndrome C. mandonis. Pollen transfer between these species is further reduced by differences in stamen exsertion that are accentuated in zones of sympatry, a pattern consistent with character displacement. CONCLUSIONS: Our results demonstrate that key differences in floral color and shape mediate a gradient of specialization in Bolivian Centropogon. Interspecific pollen transfer is further reduced by potential character displacement of a key trait. Broadly, our results have implications for understanding the hyper-diversity of Andean cloud forests, in which multiple species of the same genus frequently co-occur.

Geography of speciation affects rate of trait divergence in haemulid fishes.

Speciation and the interactions between recently diverged species are thought to be major causes of ecological and morphological divergence in evolutionary radiations. Here, we explore the extent to which geographical overlap and time since speciation may promote divergence in marine species, which represent a small fraction of currently published studies about the patterns and processes of speciation. A time-calibrated molecular phylogeny of New World haemulid fishes, a major radiation of reef and shore fishes in the tropical West Atlantic and East Pacific, reveals 21 sister species pairs, of which eight are fully sympatric and 13 are allopatric. Sister species comparisons show a non-significant relation between most of the phenotypic traits and time since divergence in allopatric taxa. Additionally, we find no difference between sympatric and allopatric pairs in the rate of divergence in colour pattern, overall body shape, or functional morphological traits associated with locomotion or feeding. However, sympatric pairs show a significant decrease in the rate of divergence in all of these traits with increasing time since their divergence, suggesting an elevated rate of divergence at the time of speciation, the effect of which attenuates as divergence time increases. Our results are consistent with an important role for geographical overlap driving phenotypic divergence early in the speciation process, but the lack of difference in rates between sympatric and allopatric pairs indicates that the interactions between closely related species are not dominant drivers of this divergence.

Reproductive ecology and isolation of Psittacanthus calyculatus and P. auriculatus mistletoes (Loranthaceae).

BACKGROUND: Relationships between floral biology and pollinator behavior are important to understanding species diversity of hemiparasitic Psittacanthus mistletoes (c. 120 species). We aimed to investigate trait divergence linked to pollinator attraction and reproductive isolation (RI) in two hummingbird-pollinated and bird-dispersed Psittacanthus species with range overlap. METHODS: We investigated the phylogenetic relationships, floral biology, pollinator assemblages, seed dispersers and host usage, and the breeding system and female reproductive success of two sympatric populations of P. calyculatus and P. auriculatus, and one allopatric population of P. calyculatus. Flowers in sympatry were also reciprocally pollinated to assess a post-mating component of RI. RESULTS: Hummingbird assemblages differed between calyculatus populations, while allopatric plants of calyculatus opened more but smaller flowers with longer lifespans and produced less nectar than those in sympatry. Bayesian-based phylogenetic analysis indicated monophyly for calyculatus populations (i.e. both populations belong to the same species). In sympatry, calyculatus plants opened more and larger flowers with longer lifespans and produced same nectar volume than those of auriculatus; populations shared pollinators but seed dispersers and host usage differed between species. Nectar standing crops differed between sympatric populations, with lower visitation in calyculatus. Hand pollination experiments indicated a predominant outcrossing breeding system, with fruit set after interspecific pollination two times higher from calyculatus to auriculatus than in the opposite direction. CONCLUSIONS: Given the low genetic differentiation between calyculatus populations, observed trait divergence could have resulted from changes regarding the local communities of pollinators and, therefore, expected divergence for peripheral, allopatric populations. Using RI estimates, there were fewer heterospecific matings than expected by chance in P. calyculatus (RI4A = 0.629) as compared to P. auriculatus (RI4A = 0.20). When considering other factors of ecological isolation that affect co-occurrence, the RI4C values indicate that isolation by hummingbird pollinators was less effective (0.20) than isolation by host tree species and seed dispersers (0.80 and 0.60, respectively), suggesting that host usage is the most important ecological isolation factor between the two species. Accordingly, the absolute and relative cumulative strength values indicated that the host tree species' barrier is currently contributing the most to maintaining these species in sympatry.

Origins of female genital diversity: Predation risk and lock-and-key explain rapid divergence during an adaptive radiation.

The study of male genital diversity has long overshadowed evolutionary inquiry of female genitalia, despite its nontrivial diversity. Here, we identify four nonmutually exclusive mechanisms that could lead to genital divergence in females, and potentially generate patterns of correlated male-female genital evolution: (1) ecological variation alters the context of sexual selection ("ecology hypothesis"), (2) sexually antagonistic selection ("sexual-conflict hypothesis"), (3) female preferences for male genitalia mediated by female genital traits ("female-choice hypothesis"), and (4) selection against inter-population mating ("lock-and-key hypothesis"). We performed an empirical investigation of all four hypotheses using the model system of Bahamas mosquitofish inhabiting blue holes that vary in predation risk. We found unequivocal support for the ecology hypothesis, with females exhibiting a smaller genital opening in blue holes containing piscivorous fish. This is consistent with stronger postmating female choice/conflict when predators are present, but greater premating female choice in their absence. Our results additionally supported the lock-and-key hypothesis, uncovering a pattern of reproductive character displacement for genital shape. We found no support for the sexual conflict or female choice hypotheses. Our results demonstrate a strong role for ecology in generating female genital diversity, and suggest that lock-and-key may provide a viable cause of female genital diversification.

Reproductive interference explains persistence of aggression between species.

Interspecific territoriality occurs when individuals of different species fight over space, and may arise spontaneously when populations of closely related territorial species first come into contact. But defence of space is costly, and unless the benefits of excluding heterospecifics exceed the costs, natural selection should favour divergence in competitor recognition until the species no longer interact aggressively. Ordinarily males of different species do not compete for mates, but when males cannot distinguish females of sympatric species, females may effectively become a shared resource. We model how reproductive interference caused by undiscriminating males can prevent interspecific divergence, or even cause convergence, in traits used to recognize competitors. We then test the model in a genus of visually orienting insects and show that, as predicted by the model, differences between species pairs in the level of reproductive interference, which is causally related to species differences in female coloration, are strongly predictive of the current level of interspecific aggression. Interspecific reproductive interference is very common and we discuss how it may account for the persistence of interspecific aggression in many taxonomic groups.

Competition for hummingbird pollination shapes flower color variation in Andean solanaceae.

One classic explanation for the remarkable diversity of flower colors across angiosperms involves evolutionary shifts among different types of pollinators with different color preferences. However, the pollinator shift model fails to account for the many examples of color variation within clades that share the same pollination system. An alternate explanation is the competition model, which suggests that color divergence evolves in response to interspecific competition for pollinators, as a means to decrease interspecific pollinator movements. This model predicts color overdispersion within communities relative to null assemblages. Here, we combine morphometric analyses, field surveys, and models of pollinator vision with a species-level phylogeny to test the competition model in the primarily hummingbird-pollinated clade Iochrominae (Solanaceae). Results show that flower color as perceived by pollinators is significantly overdispersed within sites. This pattern is not simply due to phylogenetic history: phylogenetic community structure does not deviate from random expectations, and flower color lacks phylogenetic signal. Moreover, taxa that occur in sympatry occupy a significantly larger volume of color space than those in allopatry, supporting the hypothesis that competition in sympatry drove the evolution of novel colors. We suggest that competition among close relatives may commonly underlie floral divergence, especially in species-rich habitats where congeners frequently co-occur.

Using genomic data to revisit an early example of reproductive character displacement in Haitian Anolis lizards.

The pattern of reproductive character displacement (RCD)-in which traits associated with reproductive isolation are more different where two species occur together than where they occur in isolation-is frequently attributed to reinforcement, a process during which natural selection acting against maladaptive mating events leads to enhanced prezygotic isolation between species or incipient species. One of the first studies of RCD to include molecular genetic data was described 40 years ago in a complex of Haitian trunk anole lizards using a small number of allozyme loci. In this example, Anolis caudalis appears to experience divergence in the color and pattern of an extensible throat fan, or dewlap, in areas of contact with closely related species at the northern and southern limits of its range. However, this case study has been largely overlooked for decades; meanwhile, explanations for geographic variation in dewlap color and pattern have focused primarily on adaptation to local signalling environments. We reinvestigate this example using amplified fragment length polymorphism (AFLP) genome scans, mtDNA sequence data, information on dewlap phenotypes and GIS data on environmental variation to test the hypothesis of RCD generated by reinforcement in Haitian trunk anoles. Together, our phenotypic and genetic results are consistent with RCD at the southern and northern limits of the range of A. caudalis. We evaluate the evidence for reinforcement as the explanation for RCD in Haitian trunk anoles, consider alternative explanations and provide suggestions for future work on the relationship between dewlap variation and speciation in Haitian trunk anoles.

Evidencia morfológica de hibridación entre las subespecies de Ramphocelus flammigerus (Passeriformes: Thraupidae) en Colombia / Morphological evidence of hybridization between Ramphocelus flammigerus subspecies (Passeriformes: Thraupidae) in Colombia

Morphological evidence of hybridization between Ramphocelus flammigerus subspecies (Passeriformes: Thraupidae) in Colombia. Habitat modifications such as deforestation and the increase of agricultural activities, have led to uncommon faunal interactions. In Colombia, this condition have caused the secondary contact of subspecies of Ramphocelus flammigerus populations from Cauca valley and the Pacific coast; and some specimens with rumps of intermediate colors of the subspecies have been found and are thought as hybrids. The objective of this study was to assess the presence of morphological evidence that may suggest hybridization and may explain the origin of individuals with intermediate coloration. We predict that if subspecies hybridize, they will be more similar in morphology when coexisting than when separated. Alternatively, coexisting subspecies might diverge in sympatry, because of selection to reduce competition for resources (character displacement). For this, a survey in 15 localities was undertaken: 10 allopatric areas (five for each subspecies), and five sympatric areas. Mist nets were used to capture individuals and a total of seven morphological characters were measured. To identify the patterns of morphological variation, we compared morphology of subspecies, sympatric and allopatric populations and individuals of intermediate colors. Consequently, we performed discriminant analysis and test for differences between groups by using 95% confidence intervals for log-ratio tests. A total of 112 individuals were captured (46 intermediate-colored individuals, 20 R. f. flammigerus, and 46 R. f. icteronotus. Discriminant analyses showed that subspecies were well differentiated, and intermediate individuals overlapped with them. Log-ratio test, based on Mahalanobis distances, showed that intermediate individuals were morphologically more similar to both subspecies than subspecies themselves. In addition, log-ratio tests showed that subspecies sympatric populations were similar but allopatric ones were different, and that individuals of intermediate colors were more similar to sympatric than to allopatric populations of the two subspecies. Therefore, morphological evidence supports the predictions of a hybridization hypothesis among the subspecies of R. flammigerus. In conclusion, the analysis of morphological variation in R. flammigerus suggests that hybridization between subspecies is occurring and that a process of genetic introgression is probably in progress.

Las modificaciones de los hábitats naturales, tales como la deforestación y el incremento de las actividades agrícolas, han conducido a interacciones faunísticas inusuales. En Colombia, esta situación ha generado el contacto secundario entre las poblaciones de las subespecies de Ramphocelus flammigerus del Valle del Cauca y de la costa Pacífica; y se han encontrado individuos con rabadillas de colores intermedios entre las subespecies que se han catalogado como híbridos. El objetivo del presente estudio fue evaluar si existe evidencia morfológica que sugiera hibridación y que pueda explicar el origen de los individuos de coloración intermedia. Con este fin, se obtuvieron muestras de 15 localidades; 10 zonas alopátricas (cinco por cada subespecie) y cinco zonas simpátricas. Para la captura de individuos se utilizaron redes de niebla y fueron tomados siete caracteres morfológicos. Asimismo, se predijo que si las subespecies están hibridando, las mismas, podrían ser morfológicamente más similares cuando coexisten que cuando se encuentran separadas. Alternativamente, cuando las subespecies coexisten, éstas pueden divergir en simpatría debido a presiones selectivas para reducir la competencia por recursos (desplazamiento de caracteres). Para identificar los patrones de variación morfológica, se comparó la morfología de las subespecies, de poblaciones simpátricas y alopátricas de ambas subespecies y de los individuos de cloración intermedia. Consecuentemente, se realizó un análisis discriminante y se evaluaron las diferencias entre los grupos con la utilización de intervalos de confianza del 95% para las relaciones logarítmicas. Y se capturaron un total de 112 individuos (46 de coloraciones intermedias, 20 R. f. flammigerus y 46 R. f. icteronotus). Los análisis discriminantes mostraron que las subespecies se diferencian entre ellas y que los individuos de coloraciones intermedias se traslapan con estas. Las relaciones logarítmicas, basadas en las distancias cuadradas de Mahalanobis, mostraron que los individuos intermedios fueron más similares morfológicamente a ambas subespecies que las subespecies entre ellas. Adicionalmente, se encontró que las poblaciones simpátricas de ambas subespecies son similares pero las poblaciones alopátricas son diferentes, y que los individuos de coloraciones intermedias son más similares a las poblaciones simpátricas de las dos subespecies que a las alopátricas. Por lo tanto, la evidencia morfológica evidencia las predicciones derivadas de la hipótesis de hibridación entre las subespecies de R. flammigerus. En conclusión, el análisis morfológico de la variación en R. flammigerus sugiere que se presenta hibridación entre las subespecies y que probablemente está en progreso un proceso de introgresión genética.