A multiple peak adaptive landscape based on feeding strategies and roosting ecology shaped the evolution of cranial covariance structure and morphological differentiation in phyllostomid bats

We explored the evolution of morphological integration in the most noteworthy example of adaptive radiation in mammals, the New World leaf‐nosed bats, using a massive dataset and by combining phylogenetic comparative methods and quantitative genetic approaches. We demonstrated that the phenotypic covariance structure remained conserved on a broader phylogenetic scale but also showed a substantial divergence between interclade comparisons. Most of the phylogenetic structure in the integration space can be explained by splits at the beginning of the diversification of major clades. Our results provide evidence for a multiple peak adaptive landscape in the evolution of cranial covariance structure and morphological differentiation, based upon diet and roosting ecology. In this scenario, the successful radiation of phyllostomid bats was triggered by the diversification of dietary and roosting strategies, and the invasion of these new adaptive zones lead to changes in phenotypic covariance structure and average morphology. Our results suggest that intense natural selection preceded the invasion of these new adaptive zones and played a fundamental role in shaping cranial covariance structure and morphological differentiation in this hyperdiverse clade of mammals. Finally, our study demonstrates the power of combining comparative methods and quantitative genetic approaches when investigating the evolution of complex morphologies.     

Nectar-feeding bird and bat niches in two worlds: pantropical comparisons of vertebrate pollination systems

Aim We review several aspects of the structure of regional and local assemblages of nectar‐feeding birds and bats and their relationships with food plants to determine the extent to which evolutionary convergence has or has not occurred in the New and Old World tropics. Location Our review is pantropical in extent and also includes the subtropics of South Africa and eastern Australia. Within the tropics, it deals mostly with lowland forest habitats. Methods An extensive literature review was conducted to compile data bases on the regional and local species richness of nectar‐feeding birds and bats, pollinator sizes, morphology, and diets. Coefficients of variation (CVs) were used to quantify the morphospace occupied by the various families of pollinators. The extent to which plants have become evolutionarily specialized for vertebrate pollination was explored using several criteria: number and diversity of growth forms of plant families providing food for all the considered pollinator families; the most common flower morphologies visited by all the considered pollinator families; and the number of plant families that contain genera with both bird‐ and bat‐specialized species. Results Vertebrate pollinator assemblages in the New World tropics differ from those in the Old World in terms of their greater species richness, the greater morphological diversity of their most specialized taxa, and the greater degree of taxonomic and ecological diversity and morphological specialization of their food plants. Within the Old World tropics, Africa contains more specialized nectar‐feeding birds than Asia and Australasia; Old World nectar‐feeding bats are everywhere less specialized than their New World counterparts. Main conclusions We propose that two factors – phylogenetic history and spatio‐temporal predictability (STP) of flower resources – largely account for hemispheric and regional differences in the structure of vertebrate pollinator assemblages. Greater resource diversity and resource STP in the New World have favoured the radiation of small, hovering nectar‐feeding birds and bats into a variety of relatively specialized feeding niches. In contrast, reduced resource diversity and STP in aseasonal parts of Asia as well as in Australasia have favoured the evolution of larger, non‐hovering birds and bats with relatively generalized feeding niches. Tropical Africa more closely resembles the Neotropics than Southeast Asia and Australasia in terms of resource STP and in the niche structure of its nectar‐feeding birds but not its flower‐visiting bats.     

Foraging shifts and visual preadaptation in ecologically diverse bats

Changes in behaviour may initiate shifts to new adaptive zones, with physical adaptations for novel environments evolving later. While new mutations are commonly considered engines of adaptive change, sensory evolution enabling access to new resources might also arise from standing genetic diversity, and even gene loss. We examine the relative contribution of molecular adaptations, measured by positive and relaxed selection, acting on eye‐expressed genes associated with shifts to new adaptive zones in ecologically diverse bats from the superfamily Noctilionoidea. Collectively, noctilionoids display remarkable ecological breadth, from highly divergent echolocation to flight strategies linked to specialized insectivory, the parallel evolution of diverse plant‐based diets (e.g., nectar, pollen and fruit) from ancestral insectivory, and—unusually for echolocating bats—often have large, well‐developed eyes. We report contrasting levels of positive selection in genes associated with the development, maintenance and scope of visual function, tracing back to the origins of noctilionoids and Phyllostomidae (the bat family with most dietary diversity), instead of during shifts to novel diets. Generalized plant visiting was not associated with exceptional molecular adaptation, and exploration of these novel niches took place in an ancestral phyllostomid genetic background. In contrast, evidence for positive selection in vision genes was found at subsequent shifts to either nectarivory or frugivory. Thus, neotropical noctilionoids that use visual cues for identifying food and roosts, as well as for orientation, were effectively preadapted, with subsequent molecular adaptations in nectar‐feeding lineages and the subfamily Stenodermatinae of fig‐eating bats fine‐tuning pre‐existing visual adaptations for specialized purposes.     

Cloning and Molecular Evolution of the Aldehyde Dehydrogenase 2 Gene (Aldh2) in Bats (Chiroptera)

Old World fruit bats (Pteropodidae) and New World fruit bats (Phyllostomidae) ingest significant quantities of ethanol while foraging. Mitochondrial aldehyde dehydrogenase (ALDH2, encoded by the Aldh2 gene) plays an important role in ethanol metabolism. To test whether the Aldh2 gene has undergone adaptive evolution in frugivorous and nectarivorous bats in relation to ethanol elimination, we sequenced part of the coding region of the gene (1,143 bp, ~73 % coverage) in 14 bat species, including three Old World fruit bats and two New World fruit bats. Our results showed that the Aldh2 coding sequences are highly conserved across all bat species we examined, and no evidence of positive selection was detected in the ancestral branches leading to Old World fruit bats and New World fruit bats. Further research is needed to determine whether other genes involved in ethanol metabolism have been the targets of positive selection in frugivorous and nectarivorous bats.     

Adaptive evolution in the glucose transporter 4 gene Slc2a4 in Old World fruit bats (family: Pteropodidae)

Frugivorous and nectarivorous bats are able to ingest large quantities of sugar in a short time span while avoiding the potentially adverse side-effects of elevated blood glucose. The glucose transporter 4 protein (GLUT4) encoded by the Slc2a4 gene plays a critical role in transmembrane skeletal muscle glucose uptake and thus glucose homeostasis. To test whether the Slc2a4 gene has undergone adaptive evolution in bats with carbohydrate-rich diets in relation to their insect-eating sister taxa, we sequenced the coding region of the Slc2a4 gene in a number of bat species, including four Old World fruit bats (Pteropodidae) and three New World fruit bats (Phyllostomidae). Our molecular evolutionary analyses revealed evidence that Slc2a4 has undergone a change in selection pressure in Old World fruit bats with 11 amino acid substitutions detected on the ancestral branch, whereas, no positive selection was detected in the New World fruit bats. We noted that in the former group, amino acid replacements were biased towards either Serine or Isoleucine, and, of the 11 changes, six were specific to Old World fruit bats (A133S, A164S, V377F, V386I, V441I and G459S). Our study presents preliminary evidence that the Slc2a4 gene has undergone adaptive changes in Old World fruit bats in relation to their ability to meet the demands of a high sugar diet.     

Sources of Assimilated Proteins in Old and New World Phytophagous Bats

Dietary proteins are considered crucial for growth and maintenance in mammals, but many fruit‐eating mammals feed largely on a protein‐poor diet. In the Chiroptera, frugivory has evolved twice, in the Old World Pteropodidae and in the New World Phyllostomidae, especially the Stenodermatinae. Recent studies based on the analysis of nitrogen isotope ratios (δ¹⁵N) suggest that phyllostomids feed to varying degrees on arthropods to meet their nitrogen (N) requirements. Arthropod feeding has rarely been observed in Pteropodidae. Thus, we asked whether pteropodids meet their N requirements by feeding exclusively on plant matter. We predicted that tissue from pteropodid wing membranes should be depleted in ¹⁵N relative to those of obligate insectivorous rhinolophoid, vespertilionid or emballonurid bats, if pteropodids acquire proteins exclusively from fruits, leaves or nectar. We found that δ¹⁵N in pteropodids were significantly lower than in obligate insectivorous bats. In addition, mean δ¹⁵N of Old World pteropodids was similar to that of obligate frugivorous stenodermatines of the New World tropics. We infer from these data that pteropodids are predominantly phytophagous bats. From a nutritional perspective, pteropodids and stenodermatines are very similar, suggesting that they share convergent physiological adaptations to compensate for the lack of dietary nitrogen.     

Drinking and Flying: Does Alcohol Consumption Affect the Flight and Echolocation Performance of Phyllostomid Bats?

Background

In the wild, frugivorous and nectarivorous bats often eat fermenting fruits and nectar, and thus may consume levels of ethanol that could induce inebriation. To understand if consumption of ethanol by bats alters their access to food and general survival requires examination of behavioural responses to its ingestion, as well as assessment of interspecific variation in those responses. We predicted that bats fed ethanol would show impaired flight and echolocation behaviour compared to bats fed control sugar water, and that there would be behavioural differences among species.

Methodology/Principal Findings

We fed wild caught Artibeus jamaicensis, A. lituratus, A. phaeotis, Carollia sowelli, Glossophaga soricina, and Sturnira lilium (Chiroptera, Phyllostomidae) sugar water (44 g of table sugar in 500 ml of water) or sugar water with ethanol before challenging them to fly through an obstacle course while we simultaneously recorded their echolocation calls. We used bat saliva, a non-invasive proxy, to measure blood ethanol concentrations ranging from 0 to >0.3% immediately before flight trials. Flight performance and echolocation behaviour were not significantly affected by consumption of ethanol, but species differed in their blood alcohol concentrations after consuming it.

Conclusions/Significance

The bats we studied display a tolerance for ethanol that could have ramifications for the adaptive radiation of frugivorous and nectarivorous bats by allowing them to use ephemeral food resources over a wide span of time. By sampling across phyllostomid genera, we show that patterns of apparent ethanol tolerance in New World bats are broad, and thus may have been an important early step in the evolution of frugivory and nectarivory in these animals.     

Zoogeographical regions and geospatial patterns of phylogenetic diversity and endemism of New World bats

The analysis of regional scale patterns of diversity allows insights into the processes that have shaped modern biodiversity at the macro‐scale. Previous analyses studying biogeographic regionalisation across different high‐level taxa have shown similar trends at a global scale. However, incorporating phylogenetic methods when comparing biogeographic regionalisation between subgroups facilitates identification of mechanisms leading to the biogeographic distribution of specific taxa. We analysed the spatial trends of phylogenetic diversity and phylogenetic endemism of 325 species of New World bats, using updated range maps of the modern distributions. These analyses showed phylogeographic signals that reflect the different evolutionary histories of these families. Zoogeographical zones were detected based on range‐weighted phylogenetic turnover. Values of high phylogenetic diversity and endemism were distributed differently across families, suggesting niche conservatism, but a general latitudinal trend of diversity was evident across taxa. Overall, two main bioregions were shared across New World bat taxa (Nearctic and Neotropical), with two additional subregions (Andean and La Platan). We found strong support for an additional transitional zone in the Pacific coast of South America for Emballonuridae and Molossidae. Differences in regionalisation across families indicate that niche conservatism, in situ diversification and dispersal ability are major drivers for the regionalisation of New World bats, within a dual‐centre of diversification scenario. We also found strong inter‐familial support for an independent Caribbean biogeographic region.     

Phosphoenolpyruvate Carboxykinase 1 Gene (Pck1) Displays Parallel Evolution between Old World and New World Fruit Bats

Bats are an ideal mammalian group for exploring adaptations to fasting due to their large variety of diets and because fasting is a regular part of their life cycle. Mammals fed on a carbohydrate-rich diet experience a rapid decrease in blood glucose levels during a fast, thus, the development of mechanisms to resist the consequences of regular fasts, experienced on a daily basis, must have been crucial in the evolution of frugivorous bats. Phosphoenolpyruvate carboxykinase 1 (PEPCK1, encoded by the Pck1 gene) is the rate-limiting enzyme in gluconeogenesis and is largely responsible for the maintenance of glucose homeostasis during fasting in fruit-eating bats. To test whether Pck1 has experienced adaptive evolution in frugivorous bats, we obtained Pck1 coding sequence from 20 species of bats, including five Old World fruit bats (OWFBs) (Pteropodidae) and two New World fruit bats (NWFBs) (Phyllostomidae). Our molecular evolutionary analyses of these sequences revealed that Pck1 was under purifying selection in both Old World and New World fruit bats with no evidence of positive selection detected in either ancestral branch leading to fruit bats. Interestingly, however, six specific amino acid substitutions were detected on the ancestral lineage of OWFBs. In addition, we found considerable evidence for parallel evolution, at the amino acid level, between the PEPCK1 sequences of Old World fruit bats and New World fruit bats. Test for parallel evolution showed that four parallel substitutions (Q276R, R503H, I558V and Q593R) were driven by natural selection. Our study provides evidence that Pck1 underwent parallel evolution between Old World and New World fruit bats, two lineages of mammals that feed on a carbohydrate-rich diet and experience regular periods of fasting as part of their life cycle.     

Parallel Evolution of the Glycogen Synthase 1 (Muscle) Gene Gys1 Between Old World and New World Fruit Bats (Order: Chiroptera)

Glycogen synthase, which catalyzes the synthesis of glycogen, is especially important for Old World (Pteropodidae) and New World (Phyllostomidae) fruit bats that ingest high-carbohydrate diets. Glycogen synthase 1, encoded by the Gys1 gene, is the glycogen synthase isozyme that functions in muscles. To determine whether Gys1 has undergone adaptive evolution in bats with carbohydrate-rich diets, in comparison to insect-eating sister bat taxa, we sequenced the coding region of the Gys1 gene from 10 species of bats, including two Old World fruit bats (Pteropodidae) and a New World fruit bat (Phyllostomidae). Our results show no evidence for positive selection in the Gys1 coding sequence on the ancestral Old World and the New World Artibeus lituratus branches. Tests for convergent evolution indicated convergence of the sequences and one parallel amino acid substitution (T395A) was detected on these branches, which was likely driven by natural selection.     

Colour vision variation in leaf‐nosed bats (Phyllostomidae): Links to cave roosting and dietary specialization

Bats are a diverse radiation of mammals of enduring interest for understanding the evolution of sensory specialization. Colour vision variation among species has previously been linked to roosting preferences and echolocation form in the suborder Yinpterochiroptera, yet questions remain about the roles of diet and habitat in shaping bat visual ecology. We sequenced OPN1SW and OPN1LW opsin genes for 20 species of leaf‐nosed bats (family Phyllostomidae; suborder Yangochiroptera) with diverse roosting and dietary ecologies, along with one vespertilionid species (Myotis lavali). OPN1LW genes appear intact for all species, and predicted spectral tuning of long‐wavelength opsins varied among lineages. OPN1SW genes appear intact and under purifying selection for Myotis lavali and most phyllostomid bats, with two exceptions: (a) We found evidence of ancient OPN1SW pseudogenization in the vampire bat lineage, and loss‐of‐function mutations in all three species of extant vampire bats; (b) we additionally found a recent, independently derived OPN1SW pseudogene in Lonchophylla mordax, a cave‐roosting species. These mutations in leaf‐nosed bats are independent of the OPN1SW pseudogenization events previously reported in Yinpterochiropterans. Therefore, the evolution of monochromacy (complete colour blindness) has occurred in both suborders of bats and under various evolutionary drivers; we find independent support for the hypothesis that obligate cave roosting drives colour vision loss. We additionally suggest that haematophagous dietary specialization and corresponding selection on nonvisual senses led to loss of colour vision through evolutionary sensory trade‐off. Our results underscore the evolutionary plasticity of opsins among nocturnal mammals.     

Pollination biology and floral scent chemistry of the Neotropical chiropterophilous Parkia pendula

During the past several decades, the pollination biology of Old World plant species pollinated by flying foxes and of New World plants pollinated by highly specialized nectar-feeding glossophagine bats has been studied in detail. However, little is known about Neotropical plants that are pollinated by less specialized phyllostomid bats. Therefore, we studied the pollination biology of Parkia pendula , a tree pollinated by Phyllostomus . Flowers of P. pendula are arranged in capitula, and a capitulum is composed of approximately 800 hermaphrodite flowers and 260 sterile flowers. The sterile flowers produced a total of 7.4 ml nectar per night, with a sugar concentration of 14.95%, and proline as the dominant amino acid. Nectar production is highest at dusk and ends at 03:00 h. The floral scent is dominated by monoterpenoids (97.9%), with ( E )-β-ocimene being the dominant (84.0%) compound. No sulfur compounds were detected. The capitula are heavily visited by four species of phyllostomid bats, of which Phyllostomus discolor is the most abundant (98.9%). Nectar production per capitulum is within the reported range of nectar produced by this pantropical genus (5.0–8.0 ml). This genus-wide range seems to be optimal for attracting non-specialized nectar-feeding bats and forces them to visit capitula of several trees to satisfy their dietary needs, thus increasing the probability of cross-pollination for this plant.     

The north-east-Brazilian Liana, Adenocalymna dichilum (Bignoniaceae) pollinated by bats

BACKGROUND AND AIMS: Of the set of syndromes displayed by specialized (euphilic) flowers, adaptation to pollination by bats (chiropterophily) is the least known. Accumulated new evidence reveals that this pollination mode plays a considerable role in tropical communities, especially in the neotropics. One family in which bat-pollinated species are known in several genera is the Bignoniaceae. Here is reported, for the first time, bat pollination and floral ecology in Adenocalymna dichilum (tribe Bignonieae). METHODS: Floral features of this species growing in Bahia (north-east Brazil) indicated possible chiropterophily, which was subsequently confirmed by direct observation and from photographs of bat visits. Timing of anthesis and nectar parameters were monitored in the field, and floral morphology was investigated with fixed flowers. KEY RESULTS: One to two flowers open per night on the upright, simple racemes of A. dichilum during several weeks in a 'steady state' mode. The bilabiate, cream-coloured corollas are functional for only a single night and wilt during the following day. A stout corolla, with a musky odour, and a large nectary disc with large quantities of watery nectar also conform to the syndrome. Glossophaga soricina (Glossophaginae) visited and pollinated the flowers in a trap-lining manner. Whilst hovering, the bats put their heads into the corolla mouth for less than 1 s to feed, thereby effecting the transfer of pollen which is deposited on their backs. CONCLUSIONS: Adenocalymna, a New World genus comprising approx. 50 species, exhibits floral adaptive radiation including species pollinated by bees, birds and possibly moths. The discovery of chiropterophily in A. dichilum adds another facet to the array of floral syndromes represented in the genus.     

Latitudinal gradients of species richness: a test of the geographic area hypothesis at two ecological scales

The geographic area hypothesis advances area as the primary cause of latitudinal gradients in diversity. The greater area of tropical zones, it suggests, stimulates speciation, inhibits extinction, and leads to increased species richness compared to the situation in smaller temperate and boreal zones. Because bats exhibit exceptionally strong latitudinal gradients of richness at multiple spatial scales in the New World, they are an appropriate system with which to test the geographic area hypothesis. We used range maps for 250 species of New World bats to estimate species richness in biogeographic zones at two hierarchical spatial scales: biome types and provinces. We then conducted a series of regression analyses to evaluate the ability of area to account for latitudinal gradients in species richness. However, spillover (zonal bleeding) of tropical species into extra-tropical zones may mask the species-area relationship and alter perceptions of the latitudinal gradient. To address this issue, we conducted additional analyses excluding tropical species, using a series of increasingly inclusive definitions of tropical ranges. Ecogeographic zones of the New World are not larger at tropical versus extra-tropical latitudes. Moreover, spillover of tropical species into ecogeographic zones within extra-tropical regions generally does not diminish the association between richness and area. Nonetheless, the latitudinal gradient of species richness is strong and significant at both ecogeographic scales. Clearly, area does not drive the latitudinal gradient of bat species richness in the New World. In fact, area represents a source of noise rather than a dominant signal at the focal scale of biome types and provinces in the Western Hemisphere.     

Functional performance of turtle humerus shape across an ecological adaptive landscape

The concept of the adaptive landscape has been invaluable to evolutionary biologists for visualizing the dynamics of selection and adaptation, and is increasingly being used to study morpho‐functional data. Here, we construct adaptive landscapes to explore functional trade‐offs associated with variation in humerus morphology among turtles adapted to three different locomotor environments: marine, semiaquatic, and terrestrial. Humerus shape from 40 species of cryptodire turtles was quantified using a pseudolandmark approach. Hypothetical shapes were extracted in a grid across morphospace and four functional traits (strength, stride length, mechanical advantage, and hydrodynamics) measured on those shapes. Quantitative trait modeling was used to construct adaptive landscapes that optimize the functional traits for each of the three locomotor ecologies. Our data show that turtles living in different environments have statistically different humeral shapes. The optimum adaptive landscape for each ecology is defined by a different combination of performance trade‐offs, with turtle species clustering around their respective adaptive peak. Further, species adhere to pareto fronts between marine–semiaquatic and semiaquatic–terrestrial optima, but not between marine–terrestrial. Our study demonstrates the utility of adaptive landscapes in informing the link between form, function, and ecological adaptation, and establishes a framework for reconstructing turtle ecological evolution using isolated humeri from the fossil record.     

Seasonal reliance on nectar by an insectivorous bat revealed by stable isotopes

Many animals have seasonally plastic diets to take advantage of seasonally abundant plant resources, such as fruit or nectar. Switches from insectivorous diets that are protein rich to fruits or nectar that are carbohydrate rich present physiological challenges, but are routinely done by insectivorous songbirds during migration. In contrast, insectivorous bat species are not known to switch diets to consume fruit or nectar. Here, we use carbon stable isotope ratios to establish the first known case of a temperate bat species consuming substantial quantities of nectar during spring. We show that pallid bats (Antrozous pallidus) switch from a diet indistinguishable from that of sympatric insectivorous bat species in winter (when no cactus nectar is present) to a diet intermediate between those of insectivorous bats and nectarivorous bats during the spring bloom of a bat-adapted cactus species. Combined with previous results that established that pallid bats are effective pollinators of the cardon cactus (Pachycereus pringlei), our results suggest that the interaction between pallid bats and cardon cacti represents the first-known plant-pollinator mutualism between a plant and a temperate bat. Diet plasticity in pallid bats raises questions about the degree of physiological adaptations of insectivorous bats for incorporation of carbohydrate-rich foods, such as nectar or fruit, into the diet.     

The evolution of echolocation in bats

Recent molecular phylogenies have changed our perspective on the evolution of echolocation in bats. These phylogenies suggest that certain bats with sophisticated echolocation (e.g. horseshoe bats) share a common ancestry with non-echolocating bats (e.g. Old World fruit bats). One interpretation of these trees presumes that laryngeal echolocation (calls produced in the larynx) probably evolved in the ancestor of all extant bats. Echolocation might have subsequently been lost in Old World fruit bats, only to evolve secondarily (by tongue clicking) in this family. Remarkable acoustic features such as Doppler shift compensation, whispering echolocation and nasal emission of sound each show multiple convergent origins in bats. The extensive adaptive radiation in echolocation call design is shaped largely by ecology, showing how perceptual challenges imposed by the environment can often override phylogenetic constraints.     

Historical biogeography of New World emballonurid bats (tribe Diclidurini): taxon pulse diversification

Aim To reconstruct the biogeographical history of New World emballonurid bats (tribe Diclidurini). Although bats are the second most species‐rich order of mammals, they have not contributed substantially to our understanding of the historical biogeography of mammals in the Neotropics because of a poor fossil record. In addition, being the only group of mammals that fly, bats typically have large distributions with relatively few species endemic to restricted areas that are amenable to vicariant biogeographical approaches. Location Central and South America. Methods Phylogenetic analysis for comparing trees (PACT) is a new algorithm that incorporates all spatial information from taxon area cladograms into a general area cladogram. There were nine biogeographical areas identified in Central and South America for New World emballonurid bats. Molecular dating was used to incorporate the temporal aspect of historical biogeography. This method was compared with dispersal–vicariance analysis (DIVA), which assumes vicariance as the default mode of speciation. Results Of the 45 speciation events in a fully resolved phylogeny, eight that were hypothesized by DIVA as vicariance were considered by PACT as two peripheral isolations and six within‐area events. DIVA was less parsimonious because it required six more post‐speciation dispersal events in addition to the 73 hypothesized by PACT. DIVA reconstructed a widely distributed ancestor, suggesting that most dispersal events occurred earlier, whereas the ancestral area for PACT based on character optimization was the Northern Amazon, suggesting that dispersal events were more recent phenomena. Main conclusions The general area cladogram from PACT indicated that within‐area events, and not vicariance, provide the major mode of speciation for New World emballonurid bats. There was no biological evidence supporting or rejecting sympatric speciation in New World emballonurid bats. However, the geological history, combined with fluctuations in temperature and sea level, suggested within‐area speciation in a changing and heterogeneous environment in the Northern Amazon during the Miocene. This scenario is similar to the taxon‐pulse hypothesis of biotic diversification, which posits repeated episodes of range expansions and contractions from a stable core area such as the Guiana Shield within the Northern Amazon.     

African sunbirds hover to pollinate an invasive hummingbird-pollinated plant

Why do hummingbirds hover while Old World nectar‐feeding birds perch? A unique opportunity to explore this question is presented by the invasion into Africa of a plant adapted for pollination by hovering hummingbirds. Like other hover‐pollinated plants of the New World, the flowers of the tree tobacco Nicotiana glauca lack perches and are oriented towards open space. We find that Old World nectarivores, especially the malachite sunbird, Nectarinia famosa, hover 80% of the time when taking nectar from these flowers. They hover for up to 30 s, and are able to sustain this hovering lifestyle in an area where native nectar plants are absent. Nicotiana glauca greatly increases the local abundance of sunbirds compared with uninvaded areas. In turn, flowers visited by sunbirds formed significantly more capsules and set significantly more seed than sunbird‐excluded flowers, possibly facilitating the invasion. The results suggest a prominent role for plant, rather than bird traits in determining the occurrence of hover‐pollination, begging the question of why plants adapted for hover pollination do not occur outside the New World.     

Understanding phylogenetic incongruence: lessons from phyllostomid bats

All characters and trait systems in an organism share a common evolutionary history that can be estimated using phylogenetic methods. However, differential rates of change and the evolutionary mechanisms driving those rates result in pervasive phylogenetic conflict. These drivers need to be uncovered because mismatches between evolutionary processes and phylogenetic models can lead to high confidence in incorrect hypotheses. Incongruence between phylogenies derived from morphological versus molecular analyses, and between trees based on different subsets of molecular sequences has become pervasive as datasets have expanded rapidly in both characters and species. For more than a decade, evolutionary relationships among members of the New World bat family Phyllostomidae inferred from morphological and molecular data have been in conflict. Here, we develop and apply methods to minimize systematic biases, uncover the biological mechanisms underlying phylogenetic conflict, and outline data requirements for future phylogenomic and morphological data collection. We introduce new morphological data for phyllostomids and outgroups and expand previous molecular analyses to eliminate methodological sources of phylogenetic conflict such as taxonomic sampling, sparse character sampling, or use of different algorithms to estimate the phylogeny. We also evaluate the impact of biological sources of conflict: saturation in morphological changes and molecular substitutions, and other processes that result in incongruent trees, including convergent morphological and molecular evolution. Methodological sources of incongruence play some role in generating phylogenetic conflict, and are relatively easy to eliminate by matching taxa, collecting more characters, and applying the same algorithms to optimize phylogeny. The evolutionary patterns uncovered are consistent with multiple biological sources of conflict, including saturation in morphological and molecular changes, adaptive morphological convergence among nectar‐feeding lineages, and incongruent gene trees. Applying methods to account for nucleotide sequence saturation reduces, but does not completely eliminate, phylogenetic conflict. We ruled out paralogy, lateral gene transfer, and poor taxon sampling and outgroup choices among the processes leading to incongruent gene trees in phyllostomid bats. Uncovering and countering the possible effects of introgression and lineage sorting of ancestral polymorphism on gene trees will require great leaps in genomic and allelic sequencing in this species‐rich mammalian family. We also found evidence for adaptive molecular evolution leading to convergence in mitochondrial proteins among nectar‐feeding lineages. In conclusion, the biological processes that generate phylogenetic conflict are ubiquitous, and overcoming incongruence requires better models and more data than have been collected even in well‐studied organisms such as phyllostomid bats.