Gene losses in the common vampire bat illuminate molecular adaptations to blood feeding

Feeding exclusively on blood, vampire bats represent the only obligate sanguivorous lineage among mammals. To uncover genomic changes associated with adaptations to this unique dietary specialization, we generated a new haplotype-resolved reference-quality genome of the common vampire bat (Desmodus rotundus) and screened 26 bat species for genes that were specifically lost in the vampire bat lineage. We discovered previously-unknown gene losses that relate to metabolic and physiological changes, such as reduced insulin secretion (FFAR1, SLC30A8), limited glycogen stores (PPP1R3E), and a distinct gastric physiology (CTSE). Other gene losses likely reflect the biased nutrient composition (ERN2, CTRL) and distinct pathogen diversity of blood (RNASE7). Interestingly, the loss of REP15 likely helped vampire bats to adapt to high dietary iron levels by enhancing iron excretion and the loss of the 24S-hydroxycholesterol metabolizing enzyme CYP39A1 could contribute to their exceptional cognitive abilities. Finally, losses of key cone phototransduction genes (PDE6H, PDE6C) suggest that these strictly-nocturnal bats completely lack cone-based vision. These findings enhance our understanding of vampire bat biology and the genomic underpinnings of adaptations to sanguivory.

Evolution of degrees of carnivory and dietary specialization across Mammalia and their effects on speciation

ABSTRACTConflation between omnivory and dietary generalism limits ecological and evolutionary analyses of diet, including estimating contributions to speciation and diversification. Additionally, categorizing species into qualitative dietary classes leads to information loss in these analyses. Here, we constructed two continuous variables – degree of carnivory (i.e., the position along the continuum from complete herbivory to complete carnivory) and degree of dietary specialization (i.e., the number and variety of food resources utilized) – to elucidate their histories across Mammalia, and to tease out their independent contributions to mammalian speciation. We observed that degree of carnivory significantly affected speciation rate across Mammalia, whereas dietary specialization did not. We further considered phylogenetic scale in diet-dependent speciation and saw that degree of carnivory significantly affected speciation in ungulates, carnivorans, bats, eulipotyphlans, and marsupials, while the effect of dietary specialization was only significant in carnivorans. Across Mammalia, omnivores had the lowest speciation rates. Our analyses using two different categorical diet variables led to contrasting signals of diet-dependent diversification, and subsequently different conclusions regarding diet’s macroevolutionary role. We argue that treating variables such as diet as continuous instead of categorical reduces information loss and avoids the problem of contrasting macroevolutionary signals caused by differential discretization of biologically continuous traits.

Individual and population dietary specialization decline in fin whales during a period of ecosystem shift

This study sought to estimate the effect of an anthropogenic and climate-driven change in prey availability on the degree of individual and population specialization of a large marine predator, the fin whale (Balaenoptera physalus). We examined skin biopsies from 99 fin whales sampled in the St. Lawrence Estuary (Canada) over a nine year period (1998–2006) during which environmental change was documented. We analyzed stable isotope ratios in skin and fatty acid signatures in blubber samples of whales, as well as in seven potential prey species, and diet was quantitatively assessed using Bayesian isotopic models. An abrupt change in fin whale dietary niche coincided with a decrease in biomass of their predominant prey, Arctic krill (Thysanoessa spp.). This dietary niche widening toward generalist diets occurred in nearly 60% of sampled individuals. The fin whale population, typically composed of specialists of either krill or lipid-rich pelagic fishes, shifted toward one composed either of krill specialists or true generalists feeding on various zooplankton and fish prey. This change likely reduced intraspecific competition. In the context of the current “Atlantification” of northern water masses, our findings emphasize the importance of considering individual-specific foraging tactics and not only population or group average responses when assessing population resilience or when implementing conservation measures.

Trophic specialization on unique resources in one of the most celebrated examples of sympatric speciation, Barombi Mbo crater lake cichlids

Divergent ecological selection often results in trophic niche partitioning and is one of the central processes underlying sympatric speciation. However, there are still few studies of niche partitioning in putative examples of sympatric speciation in the wild. Here we conducted the first quantitative study of dietary niche partitioning in one of the most celebrated examples of sympatric speciation, Barombi Mbo cichlids, using stomach contents and stable isotope analyses. We found little evidence for trophic niche partitioning among any Barombi Mbo cichlids, even among the nine species coexisting in sympatry in the littoral zone. Stable isotope analyses supported these conclusions of minimal dietary overlap. However, we did find extraordinary dietary specialization in some species, including spongivory and feeding on terrestrial ants, both unique feeding strategies among freshwater fishes. Stomach contents of the spongivore (Pungu maclareni) were 20% freshwater sponge, notable considering that only 0.04% of all fishes consume sponges. Overall, we conclude that while there is less trophic niche partitioning than expected among Barombi Mbo cichlids, there is evidence for dietary specialization on rare resources in support of Liem's paradox.

Diversity in olfactory receptor repertoires is associated with dietary specialization in a genus of frugivorous bat

Mammalian olfactory receptors (ORs) are a diverse family of genes encoding proteins that directly interact with environmental chemical cues. ORs evolve via gene duplication in a birth-death fashion, neofunctionalizing and pseudogenizing over time. Olfaction is a primary sense used for food detection in plant-visiting bats, but the relationship between dietary specialization and OR repertoire diversity is unclear. Within neotropical Leaf-nosed bats (Phyllostomidae), many lineages are plant specialists, and some have a distinct OR repertoire compared to insectivorous species. Yet, whether specialization on particular plant genera is associated with the evolution of specialized OR repertoires with narrower diversity has never been tested. Using targeted sequence capture, we sequenced the OR repertoires of three sympatric species of short-tailed fruit bats (Carollia), which vary in their degree of specialization on the fruits of Piper plants. We characterized orthologous versus duplicated receptors among Carollia species, and explored the diversity and redundancy of the receptor gene repertoire. At the species level, the most dedicated Piper specialist, Carollia castanea, had lower OR diversity compared to the two generalists (C. sowelli, C. perspicillata), but we discovered a few unique sets of ORs within C. castanea with high redundancy of similar gene duplicates. These unique receptors potentially enable C. castanea to detect Piper fruit odorants better than its two congeners. Carollia perspicillata, the species with the most generalist diet, had a higher diversity of intact receptors, suggesting the ability to detect a wider range of odorant molecules. Variation among ORs may be a factor in the coexistence of these sympatric species, facilitating the exploitation of different plant resources. Our study sheds light on how gene duplication and changes in OR diversity may play a role in dietary adaptations and underlies patterns of ecological interactions between bats and plants.

Genomics analysis of hexanoic acid exposure in Drosophila species

Drosophila sechellia is a dietary specialist endemic to the Seychelles islands that has evolved to consume the fruit of Morinda citrifolia. When ripe, the fruit of M. citrifolia contains octanoic acid and hexanoic acid, two medium chain fatty acid volatiles that deter and are toxic to generalist insects D. sechellia has evolved resistance to these volatiles allowing it to feed almost exclusively on this host plant. The genetic basis of octanoic acid resistance has been the focus of multiple recent studies, but the mechanisms that govern hexanoic acid resistance in <D. sechellia remain unknown. To understand how D. sechellia has evolved to specialize on M. citrifolia fruit and avoid the toxic effects of hexanoic acid, we exposed adult D. sechellia, D. melanogaster and D. simulans to hexanoic acid and performed RNA sequencing comparing their transcriptional responses to identify D. sechellia specific responses. Our analysis identified many more genes responding transcriptionally to hexanoic acid in the susceptible generalist species than in the specialist D. sechellia. Interrogation of the sets of differentially expressed genes showed that generalists regulated the expression of many genes involved in metabolism and detoxification whereas the specialist primarily downregulated genes involved in the innate immunity. Using these data we have identified interesting candidate genes that may be critically important in aspects of adaptation to their food source that contains high concentrations of HA. Understanding how gene expression evolves during dietary specialization is crucial for our understanding of how ecological communities are built and how evolution shapes trophic interactions.

Vulture genomes reveal molecular adaptations underlying obligate scavenging and low levels of genetic diversity

Obligate scavenging on dead and decaying animal matter is a rare dietary specialization that in extant vertebrates is restricted to vultures. These birds perform essential ecological services, yet many vulture species have undergone recent steep population declines and are now endangered. To test for molecular adaptations underlying obligate scavenging in vultures, and to assess whether genomic features might have contributed to their population declines, we generated high-quality genomes of the Himalayan and bearded vultures, representing both independent origins of scavenging within the Accipitridae, alongside a sister taxon, the upland buzzard. By comparing our data to published sequences from other birds, we show that the evolution of obligate scavenging in vultures has been accompanied by widespread positive selection acting on genes underlying gastric acid production, and immunity. Moreover, we find evidence of parallel molecular evolution, with amino acid replacements shared among divergent lineages of these scavengers. Our genome-wide screens also reveal that both the Himalayan and bearded vultures exhibit low levels of genetic diversity, equating to around a half of the mean genetic diversity of other bird genomes examined. However, demographic reconstructions indicate that population declines began at around the Last Glacial Maximum, predating the well-documented dramatic declines of the past three decades. Taken together, our genomic analyses imply that vultures harbour unique adaptations for processing carrion, but that modern populations are genetically depauperate and thus especially vulnerable to further genetic erosion through anthropogenic activities.

Functional Diversity of Morphologically Similar Digestive Organs in Muroidea Species

We examine possible ways of functional adjustment of morphologically similar alimentary tracts in rodents with different dietary specializations. We study the structure of stomach and gut epithelial surface as well as the features of its colonization with microorganisms in five gerbil species: Psammomys obesus, Meriones crassus, Gerbillus henleyi, G. andersoni, and G. dasyurus. Data on the morphological diversity of mucosa-associated microbiota have been obtained and confirmed by the results of previous microbiology studies. Species differences in chymus acidity associated with dietary specialization have been determined. Variations in the activity of the endoglucanase microbial enzyme, which is crucial for rodents fed on cellulose-containing food, have also been detected. The importance of microbiota for functional adaptations to various food types in rodents with morphologically similar digestive tracts has been evaluated.

Morphology of migration: Associations between wing shape, bill morphology, and migration in kingbirds (Tyrannus)

Morphology is closely linked to locomotion and diet in animals. In animals that undertake long-distance migrations, limb-morphology is under selection to maximize mobility and minimize energy expenditure. Migratory behaviors also interact with diet, such that migratory animals tend to be dietary generalists, while sedentary taxa tend to be dietary specialists. Despite a hypothesized link between migration status and morphology, phylogenetic comparative studies have yielded conflicting findings. In this study, we tested for evolutionary associations between migratory status and limb and bill morphology across kingbirds, a pan-American genus of birds with migratory, partially migratory, and sedentary taxa. We found that migratory kingbirds had longer and more pointed wings, in agreement with expectations if selection favors improved aerodynamics for long-distance migration. We also found an association between migratory status and bill shape, such that more migratory taxa had wider and deeper bills and sedentary taxa had longer bills. However, there was no difference in levels of intraspecific morphological variation among migrants, partial migrants, and residents, suggesting that dietary specialization has evolved independently of migration strategy. Evolutionary links between migration, diet, and morphology in kingbirds further strengthen ecomorphological associations that underlie long-distance seasonal movements in animals.