Opposing Responses to Scarcity Emerge from Functionally Unique Sociality Drivers.

AbstractFrom biofilms to whale pods, organisms across taxa live in groups, thereby accruing numerous diverse benefits of sociality. All social organisms, however, pay the inherent cost of increased resource competition. One expects that when resources become scarce, this cost will increase, causing group sizes to decrease. Indeed, this occurs in some species, but there are also species for which group sizes remain stable or even increase under scarcity. What accounts for these opposing responses? We present a conceptual framework, literature review, and theoretical model demonstrating that differing responses to sudden resource shifts can be explained by which sociality benefit exerts the strongest selection pressure on a particular species. We categorize resource-related benefits of sociality into six functionally distinct classes and model their effect on the survival of individuals foraging in groups under different resource conditions. We find that whether, and to what degree, the optimal group size (or correlates thereof) increases, decreases, or remains constant when resource abundance declines depends strongly on the dominant sociality mechanism. Existing data, although limited, support our model predictions. Overall, we show that across a wide diversity of taxa, differences in how group size shifts in response to resource declines can be driven by differences in the primary benefits of sociality.

Metabolic stress as a driver of life-history plasticity: flight promotes longevity and antioxidant production in monarch butterflies.

Life-history theory predicts that increased investment in traits related to reproduction will be associated with a reduced ability to invest in survival or longevity. One mechanistic explanation for this trade-off is that metabolic stress generated from current fitness activities (e.g. reproduction or locomotion) will increase somatic damage, leading to reduced longevity. Yet, there has been limited support for this damage-based hypothesis. A possible explanation is that individuals can respond to increases in metabolic stress by plastically inducing cellular maintenance responses, which may increase, rather than decrease, longevity. We tested this possibility by experimentally manipulating investment in flight activity (a metabolic stressor) in the migratory monarch butterfly (Danaus plexippus), a species whose reproductive fitness is dependent on survival through a period of metabolically intensive migratory flight. Consistent with the idea that metabolic stress stimulated investment in self-maintenance, increased flight activity enhanced monarch butterfly longevity and somatic tissue antioxidant capacity, likely at a cost to reproductive investment. Our study implicates a role for metabolic stress as a driver of life-history plasticity and supports a model where current engagement in metabolically stressful activities promotes somatic survival by stimulating investment in self-maintenance processes.

Sex-linked genetic diversity and differentiation in a globally distributed avian species complex.

Sex chromosomes often bear distinct patterns of genetic variation due to unique patterns of inheritance and demography. The processes of mutation, recombination, genetic drift and selection also influence rates of evolution on sex chromosomes differently than autosomes. Measuring such differences provides information about how these processes shape genomic variation and their roles in the origin of species. To test hypotheses and predictions about patterns of autosomal and sex-linked genomic diversity and differentiation, we measured population genetic statistics within and between populations and subspecies of the barn swallow (Hirundo rustica) and performed explicit comparisons between autosomal and Z-linked genomic regions. We first tested for evidence of low Z-linked genetic diversity and high Z-linked population differentiation relative to autosomes, then for evidence that the Z chromosome bears greater ancestry information due to faster lineage sorting. Finally, we investigated geographical clines across hybrid zones for evidence that the Z chromosome is resistant to introgression due to selection against hybrids. We found evidence that the barn swallow mating system, demographic history and linked selection each contribute to low Z-linked diversity and high Z-linked differentiation. While incomplete lineage sorting is rampant across the genome, our results indicate faster sorting of ancestral polymorphism on the Z. Finally, hybrid zone analyses indicate barriers to introgression on the Z chromosome, suggesting that sex-linked traits are important in reproductive isolation, especially in migratory divide regions. Our study highlights how selection, gene flow and demography shape sex-linked genetic diversity and underlines the relevance of the Z chromosome in speciation.

Demographic inference in barn swallows using whole-genome data shows signal for bottleneck and subspecies differentiation during the Holocene.

Accounting for historical demographic features is vital for many types of evolutionary inferences, including the estimation of divergence times between closely related populations. In barn swallow, Hirundo rustica, inferring historical population sizes and subspecies divergence times can shed light on the recent co-evolution of this species with humans. Pairwise sequentially Markovian coalescent uncovered population growth beginning on the order of one million years ago-which may reflect the radiation of the broader Hirundo genus-and a more recent population decline. Additionally, we used approximate Bayesian computation to evaluate hypotheses about recent timescale barn swallow demography, including population growth due to human commensalism, and a potential founder event associated with the onset of nesting on human structures. We found signal for a bottleneck event approximately 7,700 years ago, near the time that humans began building substantial structures, although there was considerable uncertainty associated with this estimate. Subspecies differentiation and subsequent growth occurred after the bottleneck in the best-supported model, an order of magnitude more recently than previous estimates in this system. We also compared results obtained from whole-genome sequencing versus reduced representation sequencing, finding many similar results despite substantial allelic dropout in the reduced representation data, which may have affected estimates of some parameters. This study presents the first genetic evidence of a potential barn swallow founder effect and subspecies divergence coinciding with the Holocene, which is an important step in analysing the biogeographical history of a well-known human commensal species.

Broadening the Taxonomic Breadth of Organisms in the Bio-Inspired Design Process.

(1) Generating a range of biological analogies is a key part of the bio-inspired design process. In this research, we drew on the creativity literature to test methods for increasing the diversity of these ideas. We considered the role of the problem type, the role of individual expertise (versus learning from others), and the effect of two interventions designed to increase creativity-going outside and exploring different evolutionary and ecological "idea spaces" using online tools. (2) We tested these ideas with problem-based brainstorming assignments from a 180-person online course in animal behavior. (3) Student brainstorming was generally drawn to mammals, and the breadth of ideas was affected more by the assigned problem than by practice over time. Individual biological expertise had a small but significant effect on the taxonomic breadth of ideas, but interactions with team members did not. When students were directed to consider other ecosystems and branches of the tree of life, they increased the taxonomic diversity of biological models. In contrast, going outside resulted in a significant decrease in the diversity of ideas. (4) We offer a range of recommendations to increase the breadth of biological models generated in the bio-inspired design process.

A multivariate view of the speciation continuum.

The concept of a "speciation continuum" has gained popularity in recent decades. It emphasizes speciation as a continuous process that may be studied by comparing contemporary population pairs that show differing levels of divergence. In their recent perspective article in Evolution, Stankowski and Ravinet provided a valuable service by formally defining the speciation continuum as a continuum of reproductive isolation, based on opinions gathered from a survey of speciation researchers. While we agree that the speciation continuum has been a useful concept to advance the understanding of the speciation process, some intrinsic limitations exist. Here, we advocate for a multivariate extension, the speciation hypercube, first proposed by Dieckmann et al. in 2004, but rarely used since. We extend the idea of the speciation cube and suggest it has strong conceptual and practical advantages over a one-dimensional model. We illustrate how the speciation hypercube can be used to visualize and compare different speciation trajectories, providing new insights into the processes and mechanisms of speciation. A key strength of the speciation hypercube is that it provides a unifying framework for speciation research, as it allows questions from apparently disparate subfields to be addressed in a single conceptual model.

Evolutionarily labile dispersal behavior and discontinuous habitats enhance population differentiation in island versus continentally distributed swallows.

The causes of population divergence in vagile groups remain a paradox in evolutionary biology: dispersive species should be able to colonize new areas, a prerequisite for allopatric speciation, but dispersal also facilitates gene flow, which erodes population differentiation. Strong dispersal ability has been suggested to enhance divergence in patchy habitats and inhibit divergence in continuous landscapes, but empirical support for this hypothesis is lacking. Here we compared patterns of population divergence in a dispersive clade of swallows distributed across both patchy and continuous habitats. The Pacific Swallow (Hirundo tahitica) has an insular distribution throughout Southeast Asia and the Pacific, while its sister species, the Welcome Swallow (H. neoxena), has a continental distribution in Australia. We used whole-genome data to demonstrate strong genetic structure and limited introgression among insular populations, but not among continental populations. Demographic models show that historic changes in habitat connectivity have contributed to population structure within the clade. Swallows appear to exhibit evolutionarily labile dispersal behavior in which they reduce dispersal propensity after island colonization despite retaining strong flight ability. Our data support the hypothesis that fragmented habitats enhance population differentiation in vagile groups, and suggest that labile dispersal behavior is a key mechanism underlying this pattern.

Population-level variation in parasite resistance due to differences in immune initiation and rate of response.

Closely related populations often differ in resistance to a given parasite, as measured by infection success or failure. Yet, the immunological mechanisms of these evolved differences are rarely specified. Does resistance evolve via changes to the host's ability to recognize that an infection exists, actuate an effective immune response, or attenuate that response? We tested whether each of these phases of the host response contributed to threespine sticklebacks' recently evolved resistance to their tapeworm Schistocephalus solidus. Although marine stickleback and some susceptible lake fish permit fast-growing tapeworms, other lake populations are resistant and suppress tapeworm growth via a fibrosis response. We subjected lab-raised fish from three populations (susceptible marine "ancestors," a susceptible lake population, and a resistant lake population) to a novel immune challenge using an injection of (1) a saline control, (2) alum, a generalized pro-inflammatory adjuvant that causes fibrosis, (3) a tapeworm protein extract, or (4) a combination of alum and tapeworm protein. With enough time, all three populations generated a robust fibrosis response to the alum treatments. Yet, only the resistant population exhibited a fibrosis response to the tapeworm protein alone. Thus, these populations differed in their ability to respond to the tapeworm protein but shared an intact fibrosis pathway. The resistant population also initiated fibrosis faster in response to alum, and was able to attenuate fibrosis, unlike the susceptible populations' slow but longer lasting response to alum. As fibrosis has pathological side effects that reduce fecundity, the faster recovery by the resistant population may reflect an adaptation to mitigate the costs of immunity. Broadly, our results confirm that parasite detection and immune initiation, activation speed, and immune attenuation simultaneously contribute to the evolution of parasite resistance and adaptations to infection in natural populations.

Divergent sexual signals reflect costs of local parasites.

Many closely related populations are distinguished by variation in sexual signals and this variation is hypothesized to play an important role in reproductive isolation and speciation. Within populations, there is considerable evidence that sexual signals provide information about the incidence and severity of parasite infections, but it remains unclear if variation in parasite communities across space could play a role in initiating or maintaining sexual trait divergence. To test for variation in parasite-associated selection, we compared three barn swallow subspecies with divergent sexual signals. We found that parasite community structure and host tolerance to ecologically similar parasites varied between subspecies. Across subspecies we also found that different parasites were costly in terms of male survival and reproductive success. For each subspecies, the preferred sexual signal(s) were associated with the most costly local parasite(s), indicating that divergent signals are providing relevant information to females about local parasite communities. Across subspecies, the same traits were often associated with different parasites, indicating that parasite-sexual signal links are quite flexible and may evolve relatively quickly. This study provides evidence for (1) variation in parasite communities and (2) different parasite-sexual signal links among three closely related subspecies with divergent sexual signal traits, suggesting that parasites may play an important role in initiating and/or maintaining the divergence of sexual signals among these closely related, yet geographically isolated populations.

Complete mitochondrial genomes provide current refined phylogenomic hypotheses for relationships among ten Hirundo species.

Hirundo is the most species-rich genus of the passerine swallow family (Hirundinidae) and has a cosmopolitan distribution. Here we report the complete, annotated mitochondrial genomes for 25 individuals from 10 of the 14 extant Hirundo species; these include representatives from four subspecies of the barn swallow, H. rustica. Mitogenomes were conserved in size, ranging from 18,500 to 18,700 base pairs. They all contained 13 protein-coding regions, 22 tRNAs, a control region, and large and small ribosomal subunits. Phylogenetic analysis resolved most of the relationships between the studied species and subspecies which were largely consistent with previously published trees. Several new relationships were observed within the phylogeny that could have only been discovered with the increased amount of genetic material. This study represents the largest Hirundo mitochondrial phylogeny to date, and could serve as a vital tool for other studies focusing on the evolution of the Hirundo genus.

Parasites and Host Species Barriers in Animal Hybrid Zones.

Species barriers are tested in hybrid zones when gene flow occurs between hybridizing species. Hybridization can erode species barriers, lead to the introgression of adaptive traits, or remain stable through time. Outcomes in hybrid zones are influenced by divergence between the hybridizing taxa, behavior, ecology, and geography. Parasites and pathogens play a major role in host fitness and appear to have varied impacts on species barriers in hybrid zones. We comprehensively reviewed the literature on parasitism in animal hybrid zones and present an evolutionary framework within which to consider parasite-hybrid interactions. Parasites most frequently show potential to contribute to species barrier breakdown in hybrid zones, but also frequently show potential to facilitate the maintenance of species barriers. Incorporating eco-immunology, parasite community theory, and spatiotemporal approaches will be important as genomic tools allow researchers to examine parasites and hybrid zones at greater resolution and in a diversity of natural habitats.

Using Networks to Connect Individual-Level Reproductive Behavior to Population Patterns.

We propose an application of network analysis to determine which traits and behaviors predict fertilizations within and between populations. This approach quantifies how reproductive behavior between individuals shapes patterns of selection and gene flow, filling an important gap in our understanding of the connection between evolutionary processes and emergent patterns.

Microclimate and host body condition influence mite population growth in a wild bird-ectoparasite system.

Parasite populations are never evenly distributed among the hosts they infect. Avian nest ectoparasites, such as mites, are no exception, as their distribution across the landscape is highly aggregated. It remains unclear if this pattern is driven by differences in transmission events alone, or if the environment that parasites inhabit after transmission also plays a role. Here, we experimentally examined the influence of the post-transmission microclimate, nest characteristics, and host condition on ectoparasite population growth in a bird-ectoparasite system. We infested barn swallow (Hirundo rustica erythrogaster) nests with a standardized number of Northern Fowl Mites (Ornithonyssus sylvarium) and analyzed both biotic (nestling mass, wing length, number of other arthropods present in the nest, and brood size) and abiotic (temperature, humidity, nest lining, nest dimensions, and substrate upon which the nest was built) predictors of mite population growth. Our results suggest that mite populations were most successful, in terms of growth, in nests with higher temperatures, lower humidity, few other arthropods, and hosts in good condition. We also found that nests built on wooden substrates support larger populations of mites than those constructed on metal or concrete. These findings lend insight into the factors that drive large-scale patterns of ectoparasite distributions.

Experimental manipulation of a signal trait reveals complex phenotype-behaviour coordination.

Animals use morphological signals such as ornamental traits or weaponry to mediate social interactions, and the extent of signal trait elaboration is often positively associated with reproductive success. By demonstrating relationships between signal traits and fitness, researchers often make inferences about how behaviour operates to shape those outcomes. However, detailed information about fine-scale individual behaviour, and its physiological basis, can be difficult to obtain. Here we show that experimental manipulations to exaggerate a signal trait (plumage colour) and concomitant changes in testosterone and stress-induced corticosterone levels altered social interactivity between manipulated males and their social mates. On average, darkened males did not have higher levels of interactivity than unmanipulated males; however, males who experienced a greater shift in colour (pale to dark), a larger, positive change in testosterone levels, and a dampened stress-induced corticosterone response had a larger increase in the number of interactions with their social mate post-manipulation compared to pre-manipulation. This work provides new insights into the integration and real-time flexibility of multivariate phenotypes and direct evidence for the role of social interactions in pair bond maintenance.

Transforming mentorship in STEM by training scientists to be better leaders.

Effective mentoring is a key component of academic and career success that contributes to overall measures of productivity. Mentoring relationships also play an important role in mental health and in recruiting and retaining students from groups underrepresented in STEM fields. Despite these clear and measurable benefits, faculty generally do not receive mentorship training, and feedback mechanisms and assessment to improve mentoring in academia are limited. Ineffective mentoring can negatively impact students, faculty, departments, and institutions via decreased productivity, increased stress, and the loss of valuable research products and talented personnel. Thus, there are clear incentives to invest in and implement formal training to improve mentorship in STEM fields. Here, we outline the unique challenges of mentoring in academia and present results from a survey of STEM scientists that support both the need and desire for more formal mentorship training. Using survey results and the primary literature, we identify common behaviors of effective mentors and outline a set of mentorship best practices. We argue that these best practices, as well as the key qualities of flexibility, communication, and trust, are skills that can be taught to prospective and current faculty. We present a model and resources for mentorship training based on our research, which we successfully implemented at the University of Colorado, Boulder, with graduate students and postdocs. We conclude that such training is an important and cost-effective step toward improving mentorship in STEM fields.

Non-Steroidal Anti-Inflammatory Drugs in Alzheimer's Disease and Parkinson's Disease: Reconsidering the Role of Neuroinflammation.

Alzheimer's disease (AD) and Parkinson's disease (PD) are the most common neurodegenerative diseases with age as the greatest risk factor. As the general population experiences extended life span, preparation for the prevention and treatment of these and other age-associated neurological diseases are warranted. Since epidemiological studies suggested that non-steroidal anti-inflammatory drug (NSAID) use decreased risk for AD and PD, increasing attention has been devoted to understanding the costs and benefits of the innate neuroinflammatory response to functional recovery following pathology onset. This review will provide a general overview on the role of neuroinflammation in these neurodegenerative diseases and an update on NSAID treatment in recent experimental animal models, epidemiological analyses, and clinical trials.