Behavioral repertoire of high‐shore littorinid snails reveals novel adaptations to an extreme environment

Species that inhabit high‐shore environments on rocky shores survive prolonged periods of emersion and thermal stress. Using two Hong Kong high‐shore littorinids (Echinolittorina malaccana and E. radiata) as models, we examined their behavioral repertoire to survive these variable and extreme conditions. Environmental temperatures ranged from 4°C in the cool season to 55.5°C in the hot season, with strong seasonal and daily fluctuations. In the hot season, both species allocated >35% of their activity budgets to stress‐mitigating thermoregulatory behaviors (e.g. standing, towering) and relatively small proportions to foraging (<20%) and reproduction (<10%). In the assumedly benign cool season, greater proportions (>70%) of activity budgets were allocated to stress mitigation behaviors (crevice occupation, aggregation formation). Both species exhibited multifunctional behaviors that optimized time use during their tidally‐constrained activity window in the hot season. Females mated while foraging when awash by the rising tide, and some males crawled on top of females prior to ceasing movement to form ''towers'', which have both thermoregulatory benefits and reduce searching time for mates during subsequent activity. The function of such behaviors varies in a state‐dependent manner, for example, the function of trail following changes over an activity cycle from mate searching on rising tides, to stress mitigation on falling tides (aiding aggregation formation), and to both functions through tower formation just before movement stops. Many of these behavioral responses are, therefore, multifunctional and can vary according to local conditions, allowing snails in this family to successfully colonize the extreme high‐shore environment.     

Thermal conductance and basal metabolic rate are part of a coordinated system for heat transfer regulation

Thermal conductance measures the ease with which heat leaves or enters  an organism''s body. Although the analysis of this physiological variable in relation to climatic and ecological factors can be traced to studies by Scholander and colleagues, only small advances have occurred ever since. Here, we analyse the relationship between minimal thermal conductance estimated during summer (C_min) and several ecological, climatic and geographical factors for 127 rodent species, in order to identify the exogenous factors that have potentially affected the evolution of thermal conductance. In addition, we evaluate whether there is compensation between C_min and basal metabolic rate (BMR)—in such a way that a scale-invariant ratio between both variables is equal to one—as could be expected from the Scholander–Irving model of heat transfer. Our major findings are (i) annual mean temperature is the best single predictor of mass-independent C_min. (ii) After controlling for the effect of body mass, there is a strong positive correlation between log₁₀ (C_min) and log₁₀ (BMR). Further, the slope of this correlation is close to one, indicating an almost perfect compensation between both physiological variables. (iii) Structural equation modelling indicated that C_min values are adjusted to BMR values and not the other way around. Thus, our results strongly suggest that BMR and thermal conductance integrate a coordinated system for heat regulation in endothermic animals and that summer conductance values are adjusted (in an evolutionary sense) to track changes in BMRs.     

Noise distracts foraging bats

Predators frequently must detect and localize their prey in challenging environments. Noisy environments have been prevalent across the evolutionary history of predator–prey relationships, but now with increasing anthropogenic activities noise is becoming a more prominent feature of many landscapes. Here, we use the gleaning pallid bat, Antrozous pallidus, to investigate the mechanism by which noise disrupts hunting behaviour. Noise can primarily function to mask—obscure by spectrally overlapping a cue of interest, or distract—occupy an animal''s attentional or other cognitive resources. Using band-limited white noise treatments that either overlapped the frequencies of a prey cue or did not overlap this cue, we find evidence that distraction is a primary driver of reduced hunting efficacy in an acoustically mediated predator. Under exposure to both noise types successful prey localization declined by half, search time nearly tripled, and bats used 25% more sonar pulses than when hunting in ambient conditions. Overall, the pallid bat does not seem capable of compensating for environmental noise. These findings have implications for mitigation strategies, specifically the importance of reducing sources of noise on the landscape rather than attempting to reduce the bandwidth of anthropogenic noise.     

Reproduction in deep‐sea vent shrimps is influenced by diet,with rhythms apparently unlinked to surface production

Variations in offspring production according to feeding strategies or food supply have been recognized in many animals from various ecosystems. Despite an unusual trophic structure based on non‐photosynthetic primary production, these relationships remain largely under‐studied in chemosynthetic ecosystems. Here, we use Rimicaris shrimps as a study case to explore relationships between reproduction, diets, and food supply in these environments. For that, we compared reproductive outputs of three congeneric shrimps differing by their diets. They inhabit vents located under oligotrophic waters of tropical gyres with opposed latitudes, allowing us to also examine the prevalence of phylogenetic vs environmental drivers in their reproductive rhythms. For this, we used both our original data and a compilation of published observations on the presence of ovigerous females covering various seasons over the past 35 years. We report distinct egg production trends between Rimicaris species relying solely on chemosymbiosis—R. exoculata and R. kairei—and one relying on mixotrophy, R. chacei. Besides, our data suggest a reproductive periodicity that does not correspond to seasonal variations in surface production, with substantial proportions of brooding females during the same months of the year, despite those months corresponding to either boreal winter or austral summer depending on the hemisphere. These observations contrast with the long‐standing paradigm in deep‐sea species for which periodic reproductive patterns have always been attributed to seasonal variations of photosynthetic production sinking from the surface. Our results suggest the presence of an intrinsic basis for biological rhythms in the deep sea, and bring to light the importance of having year‐round observations in order to understand the life history of vent animals.     

Staying close to home: Ecological constraints on space use and range fidelity in a mountain ungulate

Understanding patterns of animal space use and range fidelity has important implications for species and habitat conservation. For species that live in highly seasonal environments, such as mountain goats (Oreamnos americanus), spatial use patterns are expected to vary in relation to seasonal changes in environmental conditions and sex‐ or age‐specific selection pressures. To address hypotheses about sex, age, and seasonality influence on space‐use ecology, we collected GPS location data from 263 radio‐collared mountain goats (males, n = 140; females, n = 123) in coastal Alaska during 2005–2016. Location data were analyzed to derive seasonal and sex‐specific fixed‐kernel home range estimates and to quantify the degree of seasonal range and utilization distribution overlap. Overall, we determined that home range size was smallest during winter, expanded coincident with the onset of green‐up and parturition, and was largest during summer. Home range size of males and females did not differ significantly during winter, but females had larger home ranges than males during summer, a relationship that was switched during the mating season. Pairwise comparisons involving individual females across subsequent years indicated home ranges were significantly smaller during years when they gave birth to offspring. Mountain goats exhibited a strong degree of range fidelity, and 99% (n = 138) of individual animals returned to their previous year''s seasonal range with an average annual Bhattacharyya''s affinity utilization distribution overlap index of 68%. Similarity of seasonal home range utilization distributions varied in relation to sex and season in some respects. Home range overlap was highest during the summer vegetation growing season, particularly among females. These findings advance our understanding about how environmental variation and sex‐ and age‐related reproductive constraints influence space use and range fidelity among alpine ungulates. Documentation of the high degree of range fidelity among mountain goats has important conservation implications in landscapes increasingly altered by anthropogenic activities.     

A single heat-stress bout induces rapid and prolonged heat acclimation in the California mussel,Mytilus californianus

Climate change is not only causing steady increases in average global temperatures but also increasing the frequency with which extreme heating events occur. These extreme events may be pivotal in determining the ability of organisms to persist in their current habitats. Thus, it is important to understand how quickly an organism''s heat tolerance can be gained and lost relative to the frequency with which extreme heating events occur in the field. We show that the California mussel, Mytilus californianus—a sessile intertidal species that experiences extreme temperature fluctuations and cannot behaviourally thermoregulate—can quickly (in 24–48 h) acquire improved heat tolerance after exposure to a single sublethal heat-stress bout (2 h at 30 or 35°C) and then maintain this improved tolerance for up to three weeks without further exposure to elevated temperatures. This adaptive response improved survival rates by approximately 75% under extreme heat-stress bouts (2 h at 40°C). To interpret these laboratory findings in an ecological context, we evaluated 4 years of mussel body temperatures recorded in the field. The majority (approx. 64%) of consecutive heat-stress bouts were separated by 24–48 h, but several consecutive heat bouts were separated by as much as 22 days. Thus, the ability of M. californianus to maintain improved heat tolerance for up to three weeks after a single sublethal heat-stress bout significantly improves their probability of survival, as approximately 33% of consecutive heat events are separated by 3–22 days. As a sessile animal, mussels likely evolved the capability to rapidly gain and slowly lose heat tolerance to survive the intermittent, and often unpredictable, heat events in the intertidal zone. This adaptive strategy will likely prove beneficial under the extreme heat events predicted with climate change.     

Adaptive responses to cool climate promotes persistence of a non-native lizard

Successful establishment and range expansion of non-native species often require rapid accommodation of novel environments. Here, we use common-garden experiments to demonstrate parallel adaptive evolutionary response to a cool climate in populations of wall lizards (Podarcis muralis) introduced from southern Europe into England. Low soil temperatures in the introduced range delay hatching, which generates directional selection for a shorter incubation period. Non-native lizards from two separate lineages have responded to this selection by retaining their embryos for longer before oviposition—hence reducing the time needed to complete embryogenesis in the nest—and by an increased developmental rate at low temperatures. This divergence mirrors local adaptation across latitudes and altitudes within widely distributed species and suggests that evolutionary responses to climate can be very rapid. When extrapolated to soil temperatures encountered in nests within the introduced range, embryo retention and faster developmental rate result in one to several weeks earlier emergence compared with the ancestral state. We show that this difference translates into substantial survival benefits for offspring. This should promote short- and long-term persistence of non-native populations, and ultimately enable expansion into areas that would be unattainable with incubation duration representative of the native range.     

Changes in phenological events in response to a global warming scenario reveal greater adaptability of winter annual compared with summer annual arabidopsis ecotypes

Background and AimsThe impact of global warming on life cycle timing is uncertain. We investigated changes in life cycle timing in a global warming scenario. We compared Arabidopsis thaliana ecotypes adapted to the warm/dry Cape Verdi Islands (Cvi), Macaronesia, and the cool/wet climate of the Burren (Bur), Ireland, Northern Europe. These are obligate winter and summer annuals, respectively.MethodsUsing a global warming scenario predicting a 4 °C temperature rise from 2011 to approx. 2080, we produced F₁ seeds at each end of a thermogradient tunnel. Each F₁ cohort (cool and warm) then produced F₂ seeds at both ends of the thermal gradient in winter and summer annual life cycles. F₂ seeds from the winter life cycle were buried at three positions along the gradient to determine the impact of temperature on seedling emergence in a simulated winter life cycle.Key ResultsIn a winter life cycle, increasing temperatures advanced flowering time by 10.1 d °C^–1 in the winter annual and 4.9 d °C^–1 in the summer annual. Plant size and seed yield responded positively to global warming in both ecotypes. In a winter life cycle, the impact of increasing temperature on seedling emergence timing was positive in the winter annual, but negative in the summer annual. Global warming reduced summer annual plant size and seed yield in a summer life cycle.ConclusionsSeedling emergence timing observed in the north European summer annual ecotype may exacerbate the negative impact of predicted increased spring and summer temperatures on their establishment and reproductive performance. In contrast, seedling establishment of the Macaronesian winter annual may benefit from higher soil temperatures that will delay emergence until autumn, but which also facilitates earlier spring flowering and consequent avoidance of high summer temperatures. Such plasticity gives winter annual arabidopsis ecotypes a distinct advantage over summer annuals in expected global warming scenarios. This highlights the importance of variation in the timing of seedling establishment in understanding plant species responses to anthropogenic climate change.     

Heritability and Evolutionary Potential in Thermal Tolerance Traits in the Invasive Mediterranean Cryptic Species of Bemisia tabaci (Hemiptera: Aleyrodidae)

With advancing global climate change, the analysis of thermal tolerance and evolutionary potential is important in explaining the ecological adaptation and changes in the distribution of invasive species. To reveal the variation of heat resistance and evolutionary potential in the invasive Mediterranean cryptic species of Bemisia tabaci, we selected two Chinese populations—one from Harbin, N China, and one from Turpan, S China—that experience substantial heat and cold stress and conducted knockdown tests under static high- and low-temperature conditions. ANOVAs indicated significant effects of populations and sex on heat knockdown time and chill coma recovery time. The narrow-sense heritability (h ²) estimates of heat tolerance based on a parental half-sibling breeding design ranged from 0.47±0.03 to 0.51±0.06, and the estimates of cold tolerance varied from 0.33±0.07 to 0.36±0.06. Additive genetic variances were significantly different from zero for both heat and cold tolerance. These results suggest that invasive B. tabaci Mediterranean cryptic species possesses a strong ability to respond to thermal selection and develops rapid resistance to climate change.     

Indirect Effects of Impoundment on Migrating Fish: Temperature Gradients in Fish Ladders Slow Dam Passage by Adult Chinook Salmon and Steelhead

Thermal layering in reservoirs upstream from hydroelectric dams can create temperature gradients in fishways used by upstream migrating adults. In the Snake River, Washington, federally-protected adult salmonids (Oncorhynchus spp.) often encounter relatively cool water in dam tailraces and lower ladder sections and warmer water in the upstream portions of ladders. Using radiotelemetry, we examined relationships between fish passage behavior and the temperature difference between the top and bottom of ladders (∆T) at four dams over four years. Some spring Chinook salmon (O. tshawytscha) experienced ∆T ≥ 0.5 °C. Many summer and fall Chinook salmon and summer steelhead (O. mykiss) experienced ∆T ≥ 1.0 °C, and some individuals encountered ΔT > 4.0°C. As ΔT increased, migrants were consistently more likely to move down fish ladders and exit into dam tailraces, resulting in upstream passage delays that ranged from hours to days. Fish body temperatures equilibrated to ladder temperatures and often exceeded 20°C, indicating potential negative physiological and fitness effects. Collectively, the results suggest that gradients in fishway water temperatures present a migration obstacle to many anadromous migrants. Unfavorable temperature gradients may be common at reservoir-fed fish passage facilities, especially those with seasonal thermal layering or stratification. Understanding and managing thermal heterogeneity at such sites may be important for ensuring efficient upstream passage and minimizing stress for migratory, temperature-sensitive species.     

Adaptations to Hydrothermal Vent Life in Kiwa tyleri,a New Species of Yeti Crab from the East Scotia Ridge,Antarctica

Hydrothermal vents in the Southern Ocean are the physiologically most isolated chemosynthetic environments known. Here, we describe Kiwa tyleri sp. nov., the first species of yeti crab known from the Southern Ocean. Kiwa tyleri belongs to the family Kiwaidae and is the visually dominant macrofauna of two known vent sites situated on the northern and southern segments of the East Scotia Ridge (ESR). The species is known to depend on primary productivity by chemosynthetic bacteria and resides at the warm-eurythermal vent environment for most of its life; its short-range distribution away from vents (few metres) is physiologically constrained by the stable, cold waters of the surrounding Southern Ocean. Kiwa tylerihas been shown to present differential life history adaptations in response to this contrasting thermal environment. Morphological adaptations specific to life in warm-eurythermal waters, as found on – or in close proximity of – vent chimneys, are discussed in comparison with adaptations seen in the other two known members of the family (K. hirsuta, K. puravida), which show a preference for low temperature chemosynthetic environments.     

Characterizing the distribution and rates of microbial sulfate reduction at Middle Valley hydrothermal vents

Few studies have directly measured sulfate reduction at hydrothermal vents, and relatively little is known about how environmental or ecological factors influence rates of sulfate reduction in vent environments. A better understanding of microbially mediated sulfate reduction in hydrothermal vent ecosystems may be achieved by integrating ecological and geochemical data with metabolic rate measurements. Here we present rates of microbially mediated sulfate reduction from three distinct hydrothermal vents in the Middle Valley vent field along the Juan de Fuca Ridge, as well as assessments of bacterial and archaeal diversity, estimates of total biomass and the abundance of functional genes related to sulfate reduction, and in situ geochemistry. Maximum rates of sulfate reduction occurred at 90 °C in all three deposits. Pyrosequencing and functional gene abundance data revealed differences in both biomass and community composition among sites, including differences in the abundance of known sulfate-reducing bacteria. The abundance of sequences for Thermodesulfovibro-like organisms and higher sulfate reduction rates at elevated temperatures suggests that Thermodesulfovibro-like organisms may have a role in sulfate reduction in warmer environments. The rates of sulfate reduction presented here suggest that—within anaerobic niches of hydrothermal deposits—heterotrophic sulfate reduction may be quite common and might contribute substantially to secondary productivity, underscoring the potential role of this process in both sulfur and carbon cycling at vents.     

European Bison as a Refugee Species? Evidence from Isotopic Data on Early Holocene Bison and Other Large Herbivores in Northern Europe

According to the refugee species concept, increasing replacement of open steppe by forest cover after the last glacial period and human pressure had together forced European bison (Bison bonasus)—the largest extant terrestrial mammal of Europe—into forests as a refuge habitat. The consequent decreased fitness and population density led to the gradual extinction of the species. Understanding the pre-refugee ecology of the species may help its conservation management and ensure its long time survival. In view of this, we investigated the abundance of stable isotopes (δ¹³C and δ¹⁵N) in radiocarbon dated skeletal remains of European bison and other large herbivores—aurochs (Bos primigenius), moose (Alces alces), and reindeer (Rangifer tarandus)—from the Early Holocene of northern Europe to reconstruct their dietary habits and pattern of habitat use in conditions of low human influence. Carbon and nitrogen isotopic compositions in collagen of the ungulate species in northern central Europe during the Early Holocene showed significant differences in the habitat use and the diet of these herbivores. The values of the δ¹³C and δ¹⁵N isotopes reflected the use of open habitats by bison, with their diet intermediate between that of aurochs (grazer) and of moose (browser). Our results show that, despite the partial overlap in carbon and nitrogen isotopic values of some species, Early Holocene large ungulates avoided competition by selection of different habitats or different food sources within similar environments. Although Early Holocene bison and Late Pleistocene steppe bison utilized open habitats, their diets were significantly different, as reflected by their δ¹⁵N values. Additional isotopic analyses show that modern populations of European bison utilize much more forested habitats than Early Holocene bison, which supports the refugee status of the species.     

The reef-building coral Siderastrea siderea exhibits parabolic responses to ocean acidification and warming

Anthropogenic increases in atmospheric CO₂ over this century are predicted to cause global average surface ocean pH to decline by 0.1–0.3 pH units and sea surface temperature to increase by 1–4°C. We conducted controlled laboratory experiments to investigate the impacts of CO₂-induced ocean acidification (pCO₂ = 324, 477, 604, 2553 µatm) and warming (25, 28, 32°C) on the calcification rate of the zooxanthellate scleractinian coral Siderastrea siderea, a widespread, abundant and keystone reef-builder in the Caribbean Sea. We show that both acidification and warming cause a parabolic response in the calcification rate within this coral species. Moderate increases in pCO₂ and warming, relative to near-present-day values, enhanced coral calcification, with calcification rates declining under the highest pCO₂ and thermal conditions. Equivalent responses to acidification and warming were exhibited by colonies across reef zones and the parabolic nature of the corals'' response to these stressors was evident across all three of the experiment''s 30-day observational intervals. Furthermore, the warming projected by the Intergovernmental Panel on Climate Change for the end of the twenty-first century caused a fivefold decrease in the rate of coral calcification, while the acidification projected for the same interval had no statistically significant impact on the calcification rate—suggesting that ocean warming poses a more immediate threat than acidification for this important coral species.     

Foundation species' overlap enhances biodiversity and multifunctionality from the patch to landscape scale in southeastern United States salt marshes

Although there is mounting evidence that biodiversity is an important and widespread driver of ecosystem multifunctionality, much of this research has focused on small-scale biodiversity manipulations. Hence, which mechanisms maintain patches of enhanced biodiversity in natural systems and if these patches elevate ecosystem multifunctionality at both local and landscape scales remain outstanding questions. In a 17 month experiment conducted within southeastern United States salt marshes, we found that patches of enhanced biodiversity and multifunctionality arise only where habitat-forming foundation species overlap—i.e. where aggregations of ribbed mussels (Geukensia demissa) form around cordgrass (Spartina alterniflora) stems. By empirically scaling up our experimental results to the marsh platform at 12 sites, we further show that mussels—despite covering only approximately 1% of the marsh surface—strongly enhance five distinct ecosystem functions, including decomposition, primary production and water infiltration rate, at the landscape scale. Thus, mussels create conditions that support the co-occurrence of high densities of functionally distinct organisms within cordgrass and, in doing so, elevate salt marsh multifunctionality from the patch to landscape scale. Collectively, these findings suggest that patterns in foundation species'' overlap drive variation in biodiversity and ecosystem functioning within and across natural ecosystems. We therefore argue that foundation species should be integrated in our conceptual understanding of forces that moderate biodiversity–ecosystem functioning relationships, approaches for conserving species diversity and strategies to improve the multifunctionality of degraded ecosystems.     

Influence of environmental conditions at spawning sites and migration routes on adaptive variation and population connectivity in Chinook salmon

Many species that undergo long breeding migrations, such as anadromous fishes, face highly heterogeneous environments along their migration corridors and at their spawning sites. These environmental challenges encountered at different life stages may act as strong selective pressures and drive local adaptation. However, the relative influence of environmental conditions along the migration corridor compared with the conditions at spawning sites on driving selection is still unknown. In this study, we performed genome–environment associations (GEA) to understand the relationship between landscape and environmental conditions driving selection in seven populations of the anadromous Chinook salmon (Oncorhynchus tshawytscha)—a species of important economic, social, cultural, and ecological value—in the Columbia River basin. We extracted environmental variables for the shared migration corridors and at distinct spawning sites for each population, and used a Pool‐seq approach to perform whole genome resequencing. Bayesian and univariate GEA tests with migration‐specific and spawning site‐specific environmental variables indicated many more candidate SNPs associated with environmental conditions at the migration corridor compared with spawning sites. Specifically, temperature, precipitation, terrain roughness, and elevation variables of the migration corridor were the most significant drivers of environmental selection. Additional analyses of neutral loci revealed two distinct clusters representing populations from different geographic regions of the drainage that also exhibit differences in adult migration timing (summer vs. fall). Tests for genomic regions under selection revealed a strong peak on chromosome 28, corresponding to the GREB1L/ROCK1 region that has been identified previously in salmonids as a region associated with adult migration timing. Our results show that environmental variation experienced throughout migration corridors imposed a greater selective pressure on Chinook salmon than environmental conditions at spawning sites.     

Comparative Population Structure of Two Deep-Sea Hydrothermal-Vent-Associated Decapods (Chorocaris sp. 2 and Munidopsis lauensis) from Southwestern Pacific Back-Arc Basins

Studies of genetic connectivity and population structure in deep-sea chemosynthetic ecosystems often focus on endosymbiont-hosting species that are directly dependent on chemical energy extracted from vent effluent for survival. Relatively little attention has been paid to vent-associated species that are not exclusively dependent on chemosynthetic ecosystems. Here we assess connectivity and population structure of two vent-associated invertebrates—the shrimp Chorocaris sp. 2 and the squat lobster Munidopsis lauensis—that are common at deep-sea hydrothermal vents in the western Pacific. While Chorocaris sp. 2 has only been observed at hydrothermal vent sites, M. lauensis can be found throughout the deep sea but occurs in higher abundance around the periphery of active vents We sequenced mitochondrial COI genes and deployed nuclear microsatellite markers for both species at three sites in Manus Basin and either North Fiji Basin (Chorocaris sp. 2) or Lau Basin (Munidopsis lauensis). We assessed genetic differentiation across a range of spatial scales, from approximately 2.5 km to more than 3000 km. Population structure for Chorocaris sp. 2 was comparable to that of the vent-associated snail Ifremeria nautilei, with a single seemingly well-mixed population within Manus Basin that is genetically differentiated from conspecifics in North Fiji Basin. Population structure for Munidopsis lauensis was more complex, with two genetically differentiated populations in Manus Basin and a third well-differentiated population in Lau Basin. The unexpectedly high level of genetic differentiation between M. lauensis populations in Manus Basin deserves further study since it has implications for conservation and management of diversity in deep-sea hydrothermal vent ecosystems.     

Natural and Anthropogenic Hybridization in Two Species of Eastern Brazilian Marmosets (Callithrix jacchus and C. penicillata)

Animal hybridization is well documented, but evolutionary outcomes and conservation priorities often differ for natural and anthropogenic hybrids. Among primates, an order with many endangered species, the two contexts can be hard to disentangle from one another, which carries important conservation implications. Callithrix marmosets give us a unique glimpse of genetic hybridization effects under distinct natural and human-induced contexts. Here, we use a 44 autosomal microsatellite marker panel to examine genome-wide admixture levels and introgression at a natural C. jacchus and C. penicillata species border along the São Francisco River in NE Brazil and in an area of Rio de Janeiro state where humans introduced these species exotically. Additionally, we describe for the first time autosomal genetic diversity in wild C. penicillata and expand previous C. jacchus genetic data. We characterize admixture within the natural zone as bimodal where hybrid ancestry is biased toward one parental species or the other. We also show evidence that São Francisco River islands are gateways for bidirectional gene flow across the species border. In the anthropogenic zone, marmosets essentially form a hybrid swarm with intermediate levels of admixture, likely from the absence of strong physical barriers to interspecific breeding. Our data show that while hybridization can occur naturally, the presence of physical, even if leaky, barriers to hybridization is important for maintaining species genetic integrity. Thus, we suggest further study of hybridization under different contexts to set well informed conservation guidelines for hybrid populations that often fit somewhere between “natural” and “man-made.”     

Recurrent gene loss correlates with the evolution of stomach phenotypes in gnathostome history

The stomach, a hallmark of gnathostome evolution, represents a unique anatomical innovation characterized by the presence of acid- and pepsin-secreting glands. However, the occurrence of these glands in gnathostome species is not universal; in the nineteenth century the French zoologist Cuvier first noted that some teleosts lacked a stomach. Strikingly, Holocephali (chimaeras), dipnoids (lungfish) and monotremes (egg-laying mammals) also lack acid secretion and a gastric cellular phenotype. Here, we test the hypothesis that loss of the gastric phenotype is correlated with the loss of key gastric genes. We investigated species from all the main gnathostome lineages and show the specific contribution of gene loss to the widespread distribution of the agastric condition. We establish that the stomach loss correlates with the persistent and complete absence of the gastric function gene kit—H⁺/K⁺-ATPase (Atp4A and Atp4B) and pepsinogens (Pga, Pgc, Cym)—in the analysed species. We also find that in gastric species the pepsinogen gene complement varies significantly (e.g. two to four in teleosts and tens in some mammals) with multiple events of pseudogenization identified in various lineages. We propose that relaxation of purifying selection in pepsinogen genes and possibly proton pump genes in response to dietary changes led to the numerous independent events of stomach loss in gnathostome history. Significantly, the absence of the gastric genes predicts that reinvention of the stomach in agastric lineages would be highly improbable, in line with Dollo''s principle.