Evolutionary Ecology Research Articles

Correlated evolution of craniodental morphology and feeding ecology in carnivorans: a comparative analysis of jaw lever arms at tooth positions

AbstractSpecies in the mammalian order Carnivora have extremely diverse diets. The association between diet and craniodental morphology in carnivorans has been the subject of a number of studies. The distance from the jaw joint to the tooth positions may contribute to the ability to acquire and process food because it corresponds to the outlever arm when the jaw functions as a lever to generate a bite force. A shorter outlever arm relative to the inlever arm of the masticatory muscle generates a higher bite force. This study measured the distances from the jaw joint to different points of the teeth as the outlever lengths in the crania of terrestrial Carnivora species to show that outlever lengths corrected for phylogeny and a measure of the inlever length differ according to dietary habits among carnivorans. The distance from the jaw joint to the last molar was shortest in folivores, followed by aquatic prey specialists, suggesting that consumption of tough plant materials and, to some extent, aquatic prey with hard exoskeletons has favoured the evolution of a shorter outlever to allow stronger bites with enlarged molars. In contrast, among Canidae species, a shorter outlever to canines was associated with feeding on large prey, but this association was not found across carnivorans, suggesting that the correlated evolution of a shorter outlever at the canines and specialization for feeding on large prey depends on foraging and hunting behaviours. Combined, these findings provide some evidence that distances from the jaw joint to different points of the teeth are adapted to different feeding ecologies in carnivorans.

Ancestral environment determines the current reaction to ultraviolet radiation in Daphnia magna.

An individual's phenotype can be altered by direct contact with its present environment but also by environmental features experienced by previous generations, that is, parental or grandparental effects. However, the strength and direction of these transgenerational effects may be highly variable according to the ecological conditions experienced by ancestral generations. Here, we performed a reciprocal split‐brood experiment to compare transgenerational responses to the threat of ultraviolet radiation (UVR) in the zooplankter Daphnia magna, which had, or had not, been exposed to UVR for more than 150 generations. We found that the environment at which parents and grandparents were reared significantly influenced both behavior and life‐history traits of their descendants. However, such transgenerational responses differed between D. magna individuals with contrasting ancestral stress history, that is, when exposed to UVR previously unexposed individuals rapidly changed their behavior and life‐history traits, whereas individuals previously exposed to UVR showed less pronounced response when the UVR threat level relaxed. Hence, we here demonstrate an asymmetric transgenerational plasticity in response to UVR threat. The findings advance our understanding on the evolutionary ecology of such transgenerational effects and their potential role in response to changes in the local environment.

History and significance of tropical cave biology

“Nothing could possibly live there!” They said. Indeed, until recently, few specialized cave-adapted animals were known from volcanic, tropical, or oceanic island caves, and plausible theories had been put forward to explain their absence. But assume nothing in science! One must illuminate, explore, and survey habitats before declaring them barren. Our understanding of cave biology changed dramatically about 50 years ago following the serendipitous discovery of cave-adapted insects and other terrestrial arthropods in lava caves on the young oceanic islands of the Galapagos and Hawai‘i. The discovery and subsequent studies on the evolutionary ecology of cave animals have revealed a remarkable hidden fauna and created new sub-disciplines within biospeleology. Biological surveys of caves in other regions have confirmed the results developed in Hawai‘i. We now predict that, rather than being relicts trapped in caves by changing climate, animals actively colonized caves and adapted to exploit food resources wherever there were suitable subterranean voids. The physical environment in caves can be determined with great precision because the habitat is buffered by rock. Furthermore, the bizarre adaptations displayed by obligate cave animals are similar across many taxonomic groups. These two characteristics make caves nearly ideal natural laboratories for studying evolution and ecology. However, to the untrained researcher, caves can appear hostile and dangerous, and in fact, fieldwork in caves requires a unique marriage of athletic ability and science. In other words, it is exciting! Join me on a virtual tour of exploration, discovery, and research in caves during the past half-century.

Chemotactile social recognition in the blue-ringed octopus, Hapalochlaena maculosa

Social recognition is the ability of individuals in a species to differentiate among conspecifics based on their identity or biologically meaningful demographic. Despite evidence that they have sophisticated brains, complex behavioural repertoires, and acute sensory processing, surprisingly little is known about mechanisms aiding social recognition in cephalopods. This class’s unique chemotactile sense by the ventral arm surfaces gathers considerable information used in predator–prey interactions. Does it also help mediate social interactions? This study utilised 366 h of focal animal observations to assess the likelihood of Hapalochlaena maculosa, a nocturnal species, to retreat after physically contacting conspecifics based on their sex, familiarity and mating history. Females retreated from both sexes equally, while males were more likely to retreat after contacting female conspecifics. Most conspicuously, males were significantly more likely to retreat after contacting females with which they had already mated. These findings provide the first evidence for chemotactile sex discrimination and mate recognition within cephalopods, and supplement previous observations that male H. maculosa do not appear to detect the sex of conspecifics from a distance. The decision to retreat from or stay with an individual based on their sex or mating history, only after physical contact, emphasises the importance of chemotactile behaviour in octopus sensory ecology and behaviour. Furthermore, male octopuses have limited spermatophore production, and the use of chemotactile social recognition observed here may highlight the importance of reproduction, specifically sperm allocation and avoidance of sexual cannibalism, on the evolution of sensory ecology and cognition within this lineage.

PhylogatR: Phylogeographic data aggregation and repurposing.

Patterns of genetic diversity within species contain information the history of that species, including how they have responded to historical climate change and how easily the organism is able to disperse across its habitat. More than 40,000 phylogeographic and population genetic investigations have been published to date, each collecting genetic data from hundreds of samples. Despite these millions of data points, meta-analyses are challenging because the synthesis of results across hundreds of studies, each using different methods and forms of analysis, is a daunting and time-consuming task. It is more efficient to proceed by repurposing existing data and using automated data analysis. To facilitate data repurposing, we created a database (phylogatR) that aggregates data from different sources and conducts automated multiple sequence alignments and data curation to provide users with nearly ready-to-analyse sets of data for thousands of species. Two types of scientific research will be made easier by phylogatR: large meta-analyses of thousands of species that can address classic questions in evolutionary biology and ecology, and student- or citizen- science based investigations that will introduce a broad range of people to the analysis of genetic data. phylogatR enhances the value of existing data via the creation of software and web-based tools that enable these data to be recycled and reanalysed and increase accessibility to big data for research laboratories and classroom instructors with limited computational expertise and resources.

Evolutionary ecology of Miocene hominoid primates in Southeast Asia

The evolutionary history and palaeoecology of orangutans remains poorly understood until today. The restricted geographic distribution of extant Pongo indicates specific ecological needs. However, it is not clear whether these needs were shared by the great diversity of fossil pongines known from the Miocene to the Pleistocene. Here we show how niche modelling of stable carbon and oxygen isotope data of the carbonate fraction of dental enamel can be used to reconstruct the paleoecology of fossil and modern pongines and associated mammal communities. We focus on Khoratpithecus ayeyarwadyensis, a Late Miocene pongine from Myanmar and the sister clade to extant orangutans, and compare it to its associated mammal fauna and other fossil and extant pongines. The results are consistent with a vertical position high up in the canopy of a forested habitat with purely C3 vegetation for K. ayeyarwadyensis as well as the contemporaneous Sivapithecus. Although their positions in the modelled isotopic niche space look similar to the ecological niche occupied by modern Pongo, a comparison of the modelled niches within the pongine clade revealed possible differences in the use of microhabitats by the Miocene apes.

Delimiting the cryptic diversity and host preferences of Sycophila parasitoid wasps associated with oak galls using phylogenomic data.

Cryptic species diversity is a major challenge regarding the species-rich community of parasitoids attacking oak gall wasps due to a high degree of sexual dimorphism, morphological plasticity, small size and poorly known biology. As such, we know very little about the number of species present, nor the evolutionary forces responsible for generating this diversity. One hypothesis is that trait diversity in the gall wasps, including the morphology of the galls they induce, has evolved in response to selection imposed by the parasitoid community, with reciprocal selection driving diversification of the parasitoids. Using a rare, continental-scale data set of Sycophila parasitoid wasps reared from 44 species of cynipid galls from 18 species of oak across the USA, we combined mitochondrial DNA barcodes, ultraconserved elements (UCEs), morphological and natural history data to delimit putative species. Using these results, we generate the first large-scale assessment of ecological specialization and host association in this species-rich group, with implications for evolutionary ecology and biocontrol. We find most Sycophila target specific subsets of available cynipid host galls with similar morphologies, and generally attack larger galls. Our results suggest that parasitoid wasps such as Sycophila have adaptations allowing them to exploit particular host trait combinations, while hosts with contrasting traits are resistant to attack. These findings support the tritrophic niche concept for the structuring of plant-herbivore-parasitoid communities.

Periodically taken photographs reveal the effect of pollinator insects on seed set in lotus flowers

Understanding of pollination systems is an important topic for evolutionary ecology, food production, and biodiversity conservation. However, it is difficult to grasp the whole picture of an individual system, because the activity of pollinators fluctuates depending on the flowering period and time of day. In order to reveal effective pollinator taxa and timing of visitation to the reproductive success of plants under the complex biological interactions and fluctuating abiotic factors, we developed an automatic system to take photographs at 5-s intervals to get near-complete flower visitation by pollinators during the entire flowering period of selected flowers of Nelumbo nucifera and track the reproductive success of the same flowers until fruiting. Bee visits during the early morning hours of 05:00–07:59 on the second day of flowering under optimal temperatures with no rainfall or strong winds contributed strongly to seed set, with possible indirect negative effects by predators of the pollinators. Our results indicate the availability of periodic and consecutive photography system in clarifying the plant-pollinator interaction and its consequence to reproductive success of the plant. Further development is required to build a monitoring system to collect higher-resolution time-lapse images and automatically identify visiting insect species in the natural environment.

The rhesus macaque as a success story of the Anthropocene.

Of all the non-human primate species studied by researchers, the rhesus macaque (Macaca mulatta) is likely the most widely used across biological disciplines. Rhesus macaques have thrived during the Anthropocene and now have the largest natural range of any non-human primate. They are highly social, exhibit marked genetic diversity, and display remarkable niche flexibility (which allows them to live in a range of habitats and survive on a variety of diets). These characteristics mean that rhesus macaques are well-suited for understanding the links between sociality, health and fitness, and also for investigating intra-specific variation, adaptation and other topics in evolutionary ecology.

Quantifying eco‐evolutionary contributions to trait divergence in spatially structured systems

AbstractEcological and evolutionary processes can occur at similar time scales and, hence, influence one another. There has been much progress in developing metrics that quantify contributions of ecological and evolutionary components to trait change over time. However, many empirical evolutionary ecology studies document trait differentiation among populations structured in space. In both time and space, the observed differentiation in trait values among populations and communities can be the result of interactions between nonevolutionary (phenotypic plasticity, changes in the relative abundance of species) and evolutionary (genetic differentiation among populations) processes. However, the tools developed so far to quantify ecological and evolutionary contributions to trait changes are implicitly addressing temporal dynamics because they require directionality of change from an ancestral to a derived state. Identifying directionality from one site to another in spatial studies of eco‐evolutionary dynamics is not always possible and often not meaningful. We suggest three modifications to existing partitioning metrics so they allow quantifying ecological and evolutionary contributions to changes in population and community trait values across spatial locations in landscapes. Applying these spatially modified metrics to published empirical examples shows how these metrics can be used to generate new empirical insights and to facilitate future comparative analyses. The possibility of applying eco‐evolutionary partitioning metrics to populations and communities in natural landscapes is critical as it will broaden our capacity to quantify eco‐evolutionary interactions as they occur in nature.

Female blue tits sing frequently: a sex comparison of occurrence, context, and structure of song.

In species with mutual mate choice, we should expect adaptive signaling in both sexes. However, the role of female sexual signals is generally understudied. A case in point is female birdsong that has received considerably less attention than male song. This holds even for well-studied species such as the blue tit (Cyanistes caeruleus), an important model in evolutionary ecology. Although there have been anecdotal reports of female song from three populations, there are no quantitative studies on female song in this species. Here, we report systematic sampling from a population of individually marked blue tits over 3 years, revealing that females sang frequently throughout the sampling period. Notably, daytime singing of females occurred in functionally similar contexts as in males (agonistic, solo song, and alarm contexts) but females had lower song output than males and were not observed singing dawn song, while males showed long singing displays at dawn before copulations take place. Female and male song overlapped substantially in acoustic structure (i.e., same song types or peak frequency) but females had smaller individual song-type repertoires, shorter trills, and lower vocal consistency. Differential selection pressures related to functional differences in male and female song might explain the observed variation in acoustic structure. With the first quantitative study of female song in such a well-studied species, we hope to stimulate further investigations into the functions of female singing, especially in the Northern temperate zones where female song may have been overlooked, not only in this but perhaps in other monomorphic species.

Trypanosomatid Richness Among Rats, Opossums, and Dogs in the Caatinga Biome, Northeast Brazil, a Former Endemic Area of Chagas Disease.

Parasites are important components of the immense n-dimensional trophic network that connects all living beings because they, among others, forge biodiversity and deeply influence ecological evolution and host behavior. In this sense, the influence of Trypanosomatidae remains unknown. The aim of this study was to determine trypanosomatid infection and richness in rats, opossums, and dogs in the semiarid Caatinga biome. We submitted DNA samples from trypanosomatids obtained through axenic cultures of the blood of these mammals to mini exon multiplex-PCR, Sanger, and next-generation sequencing targeting the 18S rDNA gene. Phylogenetic analyses were performed to identify genetic diversity in the Trypanosomatidae family. Shannon, Simpson, equability, and beta-diversity indices were calculated per location and per mammalian host. Dogs were surveyed for trypanosomatid infection through hemocultures and serological assays. The examined mammal species of this area of the Caatinga biome exhibited an enormous trypanosomatid species/genotypes richness. Ten denoised Operational Taxonomic Units (ZOTUs), including three species (Trypanosoma cruzi, Trypanosoma rangeli and Crithidia mellificae) and one Trypanosoma sp. five genotypes/lineages (T. cruzi DTU TcI, TcII, and TcIV; T. rangeli A and B) and four DTU TcI haplotypes (ZOTU1, ZOTU2, ZOTU5, and ZOTU10 merged), as well as 13 Amplicon Sequence Variants (ASVs), including five species (T. cruzi, T. rangeli, C. mellificae, Trypanosoma dionisii, and Trypanosoma lainsoni), five genotypes/lineages (same as the ZOTUs) and six DTU TcI haplotypes (ASV, ASV1, ASV2, ASV3, ASV5 and ASV13), were identified in single and mixed infections. We observed that trypanosomatids present a broad host spectrum given that species related to a single host are found in other mammals from different taxa. Concomitant infections between trypanosomatids and new host-parasite relationships have been reported, and this immense diversity in mammals raised questions, such as how this can influence the course of the infection in these animals and its transmissibility. Dogs demonstrated a high infection rate by T. cruzi as observed by positive serological results (92% in 2005 and 76% in 2007). The absence of positive parasitological tests confirmed their poor infectivity potential but their importance as sentinel hosts of T. cruzi transmission.

The Evolution of Ecological Space in an Urban Agglomeration Based on a Suitability Evaluation and Cellular Automata Simulation

Changing and reconstructing the ecological space of urban agglomerations is inevitable for ecological conservation and a scientific problem that needs urgent attention from geography, ecology, and urban and rural planning. Using ArcGIS and other software for data processing, this study established a spatial attribute database, constructed a land use conversion matrix of the Changsha-Zhuzhou-Xiangtan (CZX) urban agglomeration’s ecological space, and quantitatively analyzed the main changes in ecological land. Using a trained cellular automata model with predicted land use in 2035 as the threshold value, the simulation research was presented by creating two simulation scenarios for the spatial distribution of land use by 2035 in the “Green Heart” area of the CZX urban agglomeration. The simulation results were compared, and the constraining role of land use suitability evaluation on ecological space evolution was analyzed. This study found that the total area of ecological space in the Green Heart area saw a rapid reduction, and it predicted that, by 2035, the total area of the CZX Green Heart area will have decreased. Comparing the two simulation scenarios proved the hypothesis that zoning ecological space reconstruction based on a land suitability evaluation can effectively protect ecological space and ensure ecological network functions are harnessed.

Resurrecting Shannon's surprise: landscape heterogeneity complements information use and population growth

Shannon's information (H) has two meanings: information and surprise (Shannon's original term.) This terminology characterizes the dual nature of H: 1) a reduction in uncertainty, and 2) heterogeneity, the enabler of surprise, for there is no information in a heterogeneity continuously homogeneous world. Embracing the dual nature of information/heterogeneity produces common ground between behavioral ecology and its sister fields: landscape, population, community and evolutionary ecology. In particular, we explore connections between variance and heterogeneity in resources distributions within landscapes and how such heterogeneity facilitates or hinders individuals' to be informed and utilize the appropriate tail of a resource distribution, and the consequences thereof. We examine both short‐ and long‐term consequences of two scenarios informed breeding habitat selection (site fidelity and conspecific prospecting). We emphasize two main conclusions: 1) the ecological role of heterogeneity to enhance the ability to discriminate between options (poor versus good breeding sites) in ecological time, and 2) how landscape heterogeneity feedbacks on the evolution information use when populations are small to ameliorate negative consequences of global change.

Quantitative Evaluation of Tactile Foraging Behavior in Pekin and Muscovy Ducks.

Ducks have developed a variety of foraging strategies that utilize touch sensitive bills to match their ecological niche within wetlands. These techniques include diving, sieving, dabbling, and grazing. Ducks exhibiting tactile specialization in foraging outperform visual and non-tactile foraging ducks in behavioral experiments and have a higher percentage of light-touch mechanoreceptor neurons expressing Piezo2 in the trigeminal ganglia. Belonging to two different tribes of Anseriformes, the well-studied tactile specialist Pekin (Tribe Anatini: Anas platyrhynchos domestica) and lesser studied Muscovy (Tribe Cairinini: Cairina moschata domestica) ducks were tested on a series of experiments to assess these birds’ functional tactile acuity. Both species of duck were able to separate out and consume edible items from increasing amounts of inedible plastiline clay distractors. They could also both be trained to associate a food reward with plastiline stimuli of differing size and shape using touch alone. However, only females of each species could learn to associate food reward with otherwise identical stimuli differing only in hardness. Pekin females performed significantly better than Muscovy females suggesting the anatomical specializations present in many Anatini may contribute to this type of tactile acuity. These findings have potential relevance in understanding the evolution of tactile ability and feeding ecology.

Effects of human activities on mountain forest in northern China during the middle Holocene

China has a long history of civilization and agriculture, and its terrestrial ecosystems have long been subjected to anthropogenic impacts. However, we lack detailed knowledge of the nature and timing of human impacts on the development of vegetation ecosystems in the mountain region of northern China during the Holocene, especially during the middle and late Neolithic periods. In this study, we used pollen and charcoal data, combined with the biomization method, from a sediment core from Mayinghai Lake to reconstruct the Holocene vegetation history of a mountain region in northern China. Considering the relatively warm and wet climatic conditions indicated by independent paleoclimate reconstructions, we conclude that our results provide a record of human impacts on the natural landscapes of the study region since ∼4.8 ka (1 ka = 1000 cal yr BP), which are mainly indicated by a decrease in the coverage of temperate deciduous forest (based on biomization scores), higher sedimentary charcoal concentrations, and an increase in the number of archaeological sites, both in the vicinity of the study site and throughout the whole of northern China. Our results provide new insights into the role of humans in the ecological evolution of this mountainous region during the Holocene, and we suggest that the impact of prehistoric humans on vegetation succession was potentially significant, which needs to be considered when using pollen records for paleoclimatic reconstruction.

Texas field crickets (Gryllus texensis) use visual cues to place learn but perform poorly when intra- and extra-maze cues conflict.

Central place foraging field crickets are an ideal system for studying the adaptive value of learning and memory, but more research is needed on ecologically relevant cognition in these invertebrates. Here, we test the visuospatial place learning of Texas field crickets (Gryllus texensis) in a radial arm maze. Our study expands previous work on G. texensis cognition for accuracy measures and extends our previous findings on females to both sexes. Additionally, our study examines whether crickets use intra- or extra-maze cues to locate a food reward using a maze rotation that puts the cues in conflict. We found that male and female crickets improved performance over trials when measured by accuracy variables but not latency variables. Thigmotaxis negatively impacted performance in both sexes. In a reward-absent trial, both male and female crickets demonstrated place memory. When intra- and extra-maze cues conflicted during a rotation trial, crickets' performance was not better than chance. Our rotation results suggest that crickets may experience reciprocal overshadowing of conflicting cues - a result most often seen in other taxa with conflicting multi-modal cues. We conclude that crickets do not rely solely on: (1) a single-cue association, (2) route-following, or (3) their own scent cues to navigate the maze. Instead, male and female Texas field crickets seem to learn the location of the reward using a combination of proximal and distal cues. The possibility to test large numbers of wild-caught or laboratory-reared individuals opens the door to future investigations on the evolutionary ecology of visuospatial learning in these invertebrates.

The correlated evolution of foraging mode and reproductive effort in lizards.

Life-history theory suggests that the optimal reproductive effort of an organism is affected by factors such as energy acquisition and predation risk. The observation that some organisms actively search for their prey and others ambush them creates the expectation of different energy needs and predation risk associated with each foraging behaviour, the so-called 'foraging-mode paradigm'. Although this paradigm has been around for decades, the empirical evidence consists of conflicting results derived from competing models based on different mechanisms. For instance, models within the foraging-mode paradigm suggest that widely foraging females have evolved low reproductive effort, because a heavy reproductive load decreases their ability to escape from predators. By contrast, a long-standing prediction of evolutionary theory indicates that organisms subject to high extrinsic mortality, should invest more in reproduction. Here, we present the first partial evidence that widely foraging species have evolved greater reproductive effort than have sit-and-wait species, which we attribute to a larger body size and greater mortality among mobile foragers. According to our findings, we propose a theoretical model that could explain the observed pattern in lizards, suggesting ways for evolutionary ecologists to test mechanistic hypotheses at the intraspecific level.

Female Java sparrows prefer high exploratory males without assortative mating

A major challenge in behavior and evolutionary ecology is to understand the evolution and maintenance of animal personality. Theory suggests that females can benefit by choosing a high-quality mate, but largely ignores the potential interaction between male and female personality during mate choice. Here, we examined the influence of exploration on mate choice by captive female Java sparrows (Lonchura oryzivora). Females preferred high exploratory males as mates rather than choosing mates according to their own exploration, and thus showed no assortative mating. Our results highlight the role of exploration of males in the mate preference of birds and suggest that mate compatibility plays minor role in the mate preference.

"Jack-of-all-trades" is parthenogenetic.

Sex is evolutionarily more costly than parthenogenesis, evolutionary ecologists therefore wonder why sex is much more frequent than parthenogenesis in the majority of animal lineages. Intriguingly, parthenogenetic individuals and species are as common as or even more common than sexuals in some major and putative ancient animal lineages such as oribatid mites and rotifers. Here, we analyzed oribatid mites (Acari: Oribatida) as a model group because these mites are ancient (early Paleozoic), widely distributed around the globe, and include a high number of parthenogenetic species, which often co‐exist with sexual oribatid mite species. There is evidence that the reproductive mode is phylogenetically conserved in oribatid mites, which makes them an ideal model to test hypotheses on the relationship between reproductive mode and species' ecological strategies. We used oribatid mites to test the frozen niche variation hypothesis; we hypothesized that parthenogenetic oribatid mites occupy narrow specialized ecological niches. We used the geographic range of species as a proxy for specialization as specialized species typically do have narrower geographic ranges than generalistic species. After correcting for phylogenetic signal in reproductive mode and demonstrating that geographic range size has no phylogenetic signal, we found that parthenogenetic lineages have a higher probability to have broader geographic ranges than sexual species arguing against the frozen niche variation hypothesis. Rather, the results suggest that parthenogenetic oribatid mite species are more generalistic than sexual species supporting the general‐purpose genotype hypothesis. The reason why parthenogenetic oribatid mite species are generalists with wide geographic range sizes might be that they are of ancient origin reflecting that they adapted to varying environmental conditions during evolutionary history. Overall, our findings indicate that parthenogenetic oribatid mite species possess a widely adapted general‐purpose genotype and therefore might be viewed as “Jack‐of‐all‐trades.”