Queen-Worker Conflict over Acceptance of Secondary Queens in Eusocial Insects.

AbstractThe coexistence of multiple reproductives in eusocial insects is widespread, yet the decisions leading to additional queen acceptance are not well understood. Unlike in vertebrates, acceptance decisions are likely controlled by the more numerous helper population rather than the parent reproductive. Yet there are likely to be queen-worker differences in acceptance criteria because workers and queens differ in their relatedness to a secondary queen. We develop a model that examines queen-worker conflict in two scenarios: accepting a queen's sister or daughter. We additionally ask how the mating frequency and split sex ratios affect the outcomes of these conflicts. Our results reveal that conflict over queen acceptance is highest in monandrous mating systems. We identify a "window of conflict" in which a queen is selected to accept her sister but her workers do not. Our result, that polyandry neutralizes conflict over acceptance thresholds, suggests that conflict suppression may be an additional contributor to the maintenance of polyandrous mating systems.

Natural selection: Fair weather cooperators.

An impressive long-term study of Greater Ani birds reveals fluctuating selection for group size. In wet years, with abundant food, larger groups enjoy greater protection from predators. In dry years, however, larger groups suffer greater nestling mortality relative to smaller groups.

Behavioral changes in senescent giant Pacific octopus (Enteroctopus dofleini) are associated with peripheral neural degeneration and loss of epithelial tissue.

Most species of octopus experience extreme physical decline after a single reproductive bout which extends over a period of days, weeks, or months before eventual death. Although outward indicators of senescence are widely recognized, comparatively little is known about physiological and neural changes accompanying terminal decline in octopuses. Here, we measured changes in behavioral response to nociceptive stimuli across the lifespan in giant Pacific octopus (GPO), Enteroctopus dofleini, held in public aquariums in the USA. Post-euthanasia, tissue was collected from arm tips, and neural and epithelial cell degeneration was quantified and compared with biopsies of arm tips from healthy, pre-reproductive GPOs. Behavioral assays showed significant changes both in low threshold mechanosensory responses and nociceptive behavioral responses beginning early in senescence and extending until euthanasia. Histology data showed that while the ratio of apoptotic cells to total cell number stayed constant between healthy and senescent GPOs, overall neural and epithelial cell density was significantly lower in terminally senescent octopuses compared with healthy controls. Our data provide new insight into the time-course and causes of sensory dysfunction in senescent cephalopods and suggest proactive welfare management should begin early in the senescence phase, well before animals enter terminal decline.

Social Behavior, Community Composition, Pathogen Strain, and Host Symbionts Influence Fungal Disease Dynamics in Salamanders.

The emerging fungal pathogen, Batrachochytrium dendrobatidis (Bd), which can cause a fatal disease called chytridiomycosis, is implicated in the collapse of hundreds of host amphibian species. We describe chytridiomycosis dynamics in two co-occurring terrestrial salamander species, the Santa Lucia Mountains slender salamander, Batrachoseps luciae, and the arboreal salamander, Aneides lugubris. We (1) conduct a retrospective Bd-infection survey of specimens collected over the last century, (2) estimate present-day Bd infections in wild populations, (3) use generalized linear models (GLM) to identify biotic and abiotic correlates of infection risk, (4) investigate susceptibility of hosts exposed to Bd in laboratory trials, and (5) examine the ability of host skin bacteria to inhibit Bd in culture. Our historical survey of 2,866 specimens revealed that for most of the early 20th century (~1920-1969), Bd was not detected in either species. By the 1990s the proportion of infected specimens was 29 and 17% (B. luciae and A. lugubris, respectively), and in the 2010s it was 10 and 17%. This was similar to the number of infected samples from contemporary populations (2014-2015) at 10 and 18%. We found that both hosts experience signs of chytridiomycosis and suffered high Bd-caused mortality (88 and 71% for B. luciae and A. lugubris, respectively). Our GLM revealed that Bd-infection probability was positively correlated with intraspecific group size and proximity to heterospecifics but not to abiotic factors such as precipitation, minimum temperature, maximum temperature, mean temperature, and elevation, or to the size of the hosts. Finally, we found that both host species contain symbiotic skin-bacteria that inhibit growth of Bd in laboratory trials. Our results provide new evidence consistent with other studies showing a relatively recent Bd invasion of amphibian host populations in western North America and suggest that the spread of the pathogen may be enabled both through conspecific and heterospecific host interactions. Our results suggest that wildlife disease studies should assess host-pathogen dynamics that consider the interactions and effects of multiple hosts, as well as the historical context of pathogen invasion, establishment, and epizootic to enzootic transitions to better understand and predict disease dynamics.

Differences in Fungal Disease Dynamics in Co-occurring Terrestrial and Aquatic Amphibians.

The fungal pathogen, Batrachochytrium dendrobatidis (Bd), has devastated biodiversity and ecosystem health and is implicated as a driver of mass amphibian extinctions. This 100-year study investigates which environmental factors contribute to Bd prevalence in a fully terrestrial species, and determines whether infection patterns differ between a fully terrestrial amphibian and more aquatic host species. We performed a historical survey to quantify Bd prevalence in 1127 Batrachoseps gregarius museum specimens collected from 1920 to 2000, and recent data from 16 contemporary (live-caught) B. gregarius populations from the southwestern slopes of the Sierra Nevada mountains in California, USA. We compared these results to Bd detection rates in 1395 historical and 1033 contemporary specimens from 10 species of anurans and 427 historical Taricha salamander specimens collected throughout the Sierra Nevada mountains. Our results indicate that Bd dynamics in the entirely terrestrial species, B. gregarius, differ from aquatic species in the same region in terms of both seasonal patterns of Bd abundance and in the possible timing of Bd epizootics.

Parental Care Alters the Egg Microbiome of Maritime Earwigs.

Recruitment of beneficial microbes to protect offspring, often reducing the energetic costs of care, is now recognized as an important component of parental care in many animals. Studies on earwigs (order Dermaptera) have revealed that removal of females from egg tending increases mortality of eggs due to fungal infections, possibly caused by changes in the bacterial microbiome on the egg surface. We used a controlled female-removal experiment to evaluate whether female nest attendance in the maritime earwig, Anisolabis maritima, influences the bacterial microbiome on the egg surface. Further, we analyzed the microbiomes of mothers and their eggs to determine if there are a core set of bacteria transferred to eggs through female care. Microbiomes were analyzed using 16S rRNA bacterial DNA sequencing, revealing that bacterial operational taxonomic unit (OTU) richness and diversity were both significantly higher for female attended versus unattended eggs. The core microbiome of adult females contained bacteria which have the potential to carry anti-fungal characteristics; these bacteria were found in higher presence and relative abundance on eggs where females were allowed to provide care. These results demonstrate that female egg attendance significantly impacts the bacterial microbiome of A. maritima eggs, and identifies specific bacteria within the egg microbiome that should be investigated further for beneficial anti-fungal properties in this system.

Evolution: How Not to Detect a Brood Parasite.

An elegant study on social parasitism in digger wasps quantifies the costs and benefits of kin recognition and shows that recognizing non-kin comes at a cost. This supports 'Crozier's paradox' of why kin recognition genes are unlikely to evolve when rare alleles are selected against.

Pathogen invasion and non-epizootic dynamics in Pacific newts in California over the last century.

Emerging infectious disease is a growing threat to global biodiversity. The infectious disease chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd) has led to the decline and extinction of hundreds of amphibian species. Severe Bd-caused epizootics have been documented in North, Central and South America-with many of the research focused on anurans. California, where Bd-related epizootics and amphibian declines have been reported, has some of the highest diversity of salamanders. After more than a decade since the first known epizootic in California, little is known about Bd disease dynamics in salamanders. Pacific newts (Genus: Taricha) are ideal study species because of their abundance, wide geographic range, occurrence in both aquatic and terrestrial habitats, and how little is known about Bd infection dynamics for this group. We conducted a retrospective study to determine the relationship between Pacific newts and the fungal pathogen. We tested 1895 specimens collected between 1889-2009 and found no evidence of Bd-infected Pacific newts until the late 1940's. Although we estimate that Bd emerged in this genus and rapidly spread geographically throughout California, we did not find evidence for epizootic dynamics. Bd infection prevalence and intensity, two measures commonly used to estimate dynamics, remained consistently low over time; suggesting Pacific newts may not be highly susceptible. Also, we found the timing of first Bd emergence in Pacific newts predate Bd emergence in other California salamander species. In addition, we found several environmental and anthropogenic factors correlated with Bd prevalence which may help explain Bd disease dynamics in the genus Taricha. Pacific newts may be a reservoir species that signal pathogen invasion into California salamanders, though further studies are needed.

Skin Microbiomes of California Terrestrial Salamanders Are Influenced by Habitat More Than Host Phylogeny.

A multitude of microorganisms live on and within plant and animal hosts, yet the ecology and evolution of these microbial communities remains poorly understood in many taxa. This study examined the extent to which environmental factors and host taxonomic identity explain microbiome variation within two salamander genera, Ensatina and Batrachoseps, in the family Plethodontidae. In particular, we assessed whether microbiome differentiation paralleled host genetic distance at three levels of taxonomy: genus and high and low clade levels within Ensatina eschscholtzii. We predicted that more genetically related host populations would have more similar microbiomes than more distantly related host populations. We found that salamander microbiomes possess bacterial species that are most likely acquired from their surrounding soil environment, but the relative representation of those bacterial species is significantly different on the skin of salamanders compared to soil. We found differences in skin microbiome alpha diversity among Ensatina higher and lower clade groups, as well as differences between Ensatina and Batrachoseps. We also found that relative microbiome composition (beta diversity) did vary between Ensatina lower clades, but differences were driven by only a few clades and not correlated to clade genetic distances. We conclude this difference was likely a result of Ensatina lower clades being associated with geographic location and habitat type, as salamander identity at higher taxonomic levels (genus and Ensatina higher clades) was a weak predictor of microbiome composition. These results lead us to conclude that environmental factors are likely playing a more significant role in salamander cutaneous microbiome assemblages than host-specific traits.

Mechanisms of aggregation in an ant-tended treehopper: Attraction to mutualists is balanced by conspecific competition.

Understanding the spatial structure of populations and communities has been a dominant focus of ecological research, and spatial structure is increasingly seen as critical for understanding population dynamics. Habitat (or host) preference is a proximate mechanism that can generate aggregation or overdispersion, lending insight into the ultimate consequences of observed spatial distributions. Publilia concava is a univoltine phloem-feeding insect that forms mutualistic associations with ants, which consume honeydew and protect treehoppers from predation. Treehopper adults and nymphs are aggregated at the scale of goldenrod plant stems, and previous studies have suggested that this aggregation is an adaptive response that increases feeding performance or maximizes benefits of ant-tending. Previous studies have also shown experimentally that individual treehoppers preferentially oviposit on plants with ants present, but a complimentary hypothesis that treehoppers prefer to oviposit near conspecifics (e.g., to take advantage of density-dependent ant attraction) remains untested. We show that, as expected, the probability of treehopper oviposition increases with ant-presence and relative ant abundance. However, we also find that treehopper oviposition decreases with increasing treehopper density. Thus our results are inconsistent with the hypothesis that treehopper aggregation is a socially cooperative strategy to attract ants; we suggest that aggregation is a form of conflict and an unavoidable by-product of individual responses to ant-tending levels.

Intraspecific Variation in the Skin-Associated Microbiome of a Terrestrial Salamander.

Resident microbial communities living on amphibian skin can have significant effects on host health, yet the basic ecology of the host-microbiome relationship of many amphibian taxa is poorly understood. We characterized intraspecific variation in the skin microbiome of the salamander Ensatina eschscholtzii xanthoptica, a subspecies composed of four genetically distinct populations distributed throughout the San Francisco Bay Area and the Sierra Nevada mountains in California, USA. We found that salamanders from four geographically and genetically isolated populations harbor similar skin microbial communities, which are dominated by a common core set of bacterial taxa. Additionally, within a population, the skin microbiome does not appear to differ significantly between salamanders of different ages or sexes. In all cases, the salamander skin microbiomes were significantly different from those of the surrounding terrestrial environment. These results suggest that the relationship between E. e. xanthoptica salamanders and their resident skin microbiomes is conserved, possibly indicating a stable mutualism between the host and microbiome.

Synthesizing perspectives on the evolution of cooperation within and between species.

Cooperation is widespread both within and between species, but are intraspecific and interspecific cooperation fundamentally similar or qualitatively different phenomena? This review evaluates this question, necessary for a general understanding of the evolution of cooperation. First, we outline three advantages of cooperation relative to noncooperation (acquisition of otherwise inaccessible goods and services, more efficient acquisition of resources, and buffering against variability), and predict when individuals should cooperate with a conspecific versus a heterospecific partner to obtain these advantages. Second, we highlight five axes along which heterospecific and conspecific partners may differ: relatedness and fitness feedbacks, competition and resource use, resource-generation abilities, relative evolutionary rates, and asymmetric strategy sets and outside options. Along all of these axes, certain asymmetries between partners are more common in, but not exclusive to, cooperation between species, especially complementary resource use and production. We conclude that cooperation within and between species share many fundamental qualities, and that differences between the two systems are explained by the various asymmetries between partners. Consideration of the parallels between intra- and interspecific cooperation facilitates application of well-studied topics in one system to the other, such as direct benefits within species and kin-selected cooperation between species, generating promising directions for future research.

Evolution of Conspecific Brood Parasitism versus Cooperative Breeding as Alternative Reproductive Tactics.

Cooperative breeding and conspecific brood parasitism can both be favored by ecological saturation of breeding territories or nest sites. Here, we develop a model that links these alternative reproductive tactics by focusing on nonnesting females (S) that either breed cooperatively with a nesting female (N) or parasitize a third, outside host female (H). We find that cooperative breeding is more likely to evolve with increasing relatedness of cooperating females (S or N) to the outside host female (H) and with increasing costs to the hosts for receiving parasitic eggs. Conversely, cooperation is less likely with increasing kinship between the two potentially cooperative nesters (S and N). This is because even the nesting female gains higher inclusive fitness as long as the number of parasitic eggs (of her otherwise potentially cooperating partner) is sufficiently high. We find the relationship between kinship and reproductive skew within cooperative nests can be either positive or negative depending on the fecundity of parasites versus nesting females. We also find that either of the cooperatively nesting females is more likely to tolerate a smaller fraction of group reproduction as kinship with the host female increases and as the host reproduces more (relative to the parasite) in outside nests. Finally, our model predicts that, as the outside option of conspecific brood parasitism becomes more profitable, helping behavior (zero reproduction by one female) is less likely to evolve in cooperatively breeding groups.

Asymmetric forceps increase fighting success among males of similar size in the maritime earwig.

Extreme asymmetric morphologies are hypothesized to serve an adaptive function that counteracts sexual selection for symmetry. However direct tests of function for asymmetries are lacking, particularly in the context of animal weapons. The weapon of the maritime earwig, Anisolabis maritima, exhibits sizeable variation in the extent of directional asymmetry within and across body sizes, making it an ideal candidate for investigating the function of asymmetry. In this study, we characterized the extent of weapon asymmetry, characterized the manner in which asymmetric weapons are used in contests, staged dyadic contests between males of different size classes and analyzed the correlates of fighting success. In contests between large males, larger individuals won more fights and emerged as the dominant male. In contests between small males, however, weapon asymmetry was more influential in predicting overall fighting success than body size. This result reveals an advantage of asymmetric weaponry among males that are below the mean size in the population. A forceps manipulation experiment suggests that asymmetry may be an indirect, correlate of a morphologically independent factor that affects fighting ability.

The Evolution of Intraspecific Brood Parasitism in Birds and Insects.

Many species of birds and insects engage in intraspecific brood parasitism (IBP), when a female lays eggs in the nest of a conspecific and leaves without providing parental care. These visiting females may also act to cooperate with a primary female, staying to provide parental care. Therefore, IBP and cooperative breeding can be considered extremes on a continuum of parental care provided by a secondary female. When a secondary female abandons a nest, she creates an asymmetry in parental care between herself and the host. While models of asymmetry in reproductive allocation have focused directly on relatedness between females, we lack an appropriate theoretical framework that addresses the effects of relatedness on parental care asymmetry. Here, I present an evolutionarily stable strategy (ESS) model that predicts the conditions under which IBP is favored over cooperation and solitary breeding. Intraspecific brood parasitism is less likely to evolve (relative to cooperation and solitary breeding) as the relatedness between a host and parasite increases. It can evolve, however, if parasites achieve a high overall fecundity relative to solitary females. Constraints on solitary breeding can further promote IBP under some circumstances. Cooperation is favored when relatedness is high and reproductive skew is low. This model makes several predictions regarding the conditions under which IBP may evolve, motivating a variety of experimental approaches.