Explore the vast range of titles available.

The advent of relatively inexpensive tools for characterizing microbial communities has led to an explosion of research exploring the diversity, ecology, and evolution of microbe-host systems. Some now question whether existing conceptual frameworks are adequate to explain microbe-host systems. One popular paradigm is the “holobiont-hologenome,” which argues that a host and its microbiome evolve as a single cooperative unit of selection (i.e., a superorganism). We argue that the hologenome is based on overly restrictive assumptions which render it an approach of little research utility. A host plus its microbiome is more effectively viewed as an ecological community of organisms that encompasses a broad range of interactions (parasitic to mutualistic), patterns of transmission (horizontal to vertical), and levels of fidelity among partners. The hologenome requires high partner fidelity if it is to evolve as a unit. However, even when this is achieved by particular host-microbe pairs, it is unlikely to hold for the entire host microbiome, and therefore the community is unlikely to evolve as a hologenome. Both mutualistic and antagonistic (fitness conflict) evolution can occur among constituent members of the community, not just adaptations at the “hologenome” level, and there is abundant empirical evidence for such divergence of selective interests among members of host-microbiome communities. We believe that the concepts and methods of ecology, genetics, and evolutionary biology will continue to provide a well-grounded intellectual framework for researching host-microbiome communities, without recourse to the limiting assumption that selection acts predominantly at the holobiont level.

Sustaining beneficial gut symbioses presents a major challenge for animals, including holometabolous insects. Social insects may meet such challenges through partner fidelity, aided by behavioral symbiont transfer and transgenerational inheritance through colony founders. We address such potential through colony-wide explorations across 13 eusocial, holometabolous insect species in the ant genus Cephalotes. Through amplicon sequencing, we show that previously characterized worker microbiomes are conserved in soldier castes, that adult microbiomes exhibit trends of phylosymbiosis, and that Cephalotes cospeciate with their most abundant adult-enriched symbiont. We find, also, that winged queens harbor worker-like microbiomes prior to colony founding, suggesting vertical inheritance as a means of partner fidelity. Whereas some adult-abundant symbionts colonize larvae, larval gut microbiomes are uniquely characterized by environmental bacteria from the Enterobacteriales, Lactobacillales, and Actinobacteria. Distributions across Cephalotes larvae suggest more than 40 million years of conserved environmental filtering and, thus, a second sustaining mechanism behind an ancient, developmentally partitioned symbiosis.

Using mark-resight data, we investigated fidelity to territory and mate as well as breeding dispersal rates and the causes and consequences of breeding dispersal in a 20-year study of American goshawks ( Astur atricapillus ) in Arizona, USA. Generalized Additive Mixed Models were used to identify the relative contributions of four prominent explanatory variables (eggs laid, nest failed, nest successful, mate loss) and 21 individual and environmental variables in a machine learning Conditional Inference Forest to predict breeding dispersal. Ninety-five percent of males and 92% of females exhibited lifetime territory fidelity and 97% exhibited lifetime mate fidelity. Mate loss alone (to divorce, possible emigration or death) made the biggest difference in the predicted probability of dispersal (0.11 with mate loss, 0.005 with mate retention). Yet, in 80% of mate losses a hawk stayed on its territory to eventually nest with a new mate. Territory fidelity was highest when the mate was retained in the next breeding and the pair’s previous attempt produced fledglings. All males and 86% of females that dispersed to a territory in our study area moved no farther than to a 3rd-order neighboring territory (crossed 2 territories). Despite equivocal evidence of dispersal to territories more frequently occupied by egg-layers, there was otherwise little evidence that hawks on average dispersed to better territories. On average reproduction did not improve post-dispersal and dispersers did not move to territories with greater total (all monitored yrs) reproduction. Goshawks losing their mates appeared to use a home-based mate searching that minimized loss of a familiar territory by waiting on their territory for a new mate and prospecting nearby territories for unpaired mates. The small sample of nearby prospected territories, combined with fortuitous occurrences of unpaired mates, resulted in random (with respect to quality) selections of territories by dispersers.

Obligate co-dependence can arise in symbiosis, yielding heritable partnerships. These interactions are considered to be highly specific, but partner fidelity is difficult to quantify owing to the experimental constraints of symbiont exchange between host species. Here, we overcome this challenge by leveraging the unique transmission dynamics of Stammera capleta , the obligate digestive symbiont of tortoise beetles (Chrysomelidae: Cassidinae). Despite its extracellular localization, S. capleta possesses a drastically reduced genome ( ~ 0.25 Mb) and is vertically transmitted through egg-associated spheres. Manipulating these spheres allowed us to experimentally exchange S. capleta between beetle species to determine their impact on host development. We show that non-native S. capleta can successfully colonize the symbiotic organs of a novel host, but that the interaction outcome correlates with genetic relatedness to the native symbiont. Genetically distant species trigger a more pronounced transcriptional response and can only partially rescue host development. While more closely related symbionts proliferate similarly to the native one and induce a comparable host response, they fail to propagate to the next generation, underscoring how transmission fidelity, host-symbiont compatibility, and local adaptation can further specificity within a Paleocene-aged partnership. Symbioses can form heritable partnerships, yet assessing partner fidelity remains difficult owing to limited symbiont exchange. This study shows how genetic compatibility, transmission fidelity, and local adaptation stabilize co-diversified symbioses.

As urbanization reduces species’ habitats and population sizes, managers need information on whether within-population processes, such as changes in mate and nest-site fidelity and dispersal distances, may be contributing to declines. Few avian studies have examined changes in these behaviors in declining populations or in urban settings. We investigated whether mate fidelity, nest-site fidelity or breeding dispersal distance changed over time in a population of burrowing owls ( Athene cunicularia ), a short-lived, socially-monogamous species. During the 18-year period of the study, the population declined by 69% in urban Santa Clara County, California, USA--a region of rapid urbanization. We assessed whether these behaviors were influenced by key factors including age, breeding success in the previous year, and years with the same mate, and examined the relationship between mate and nest-site fidelity over time and annual reproductive success. Our analyses showed no change over time in mate fidelity rates, nest-site fidelity rates, dispersal distances or annual reproductive success, indicating these behaviors remained stable even during a severe population decline. Although burrowing owls are a short-lived species, we found that increasing years with the same mate resulted in increased nest-site fidelity and annual reproductive success. To achieve increasing annual reproductive success in this species and others with similar fidelity behaviors, nest sites and pairs must be protected over many years allowing mates to stay together in the same nest territory. Since these fidelity behaviors were maintained during the population decline, other factors require investigation to determine the causes for decreases in this population. Burrowing owls are an urban-adaptable species that can maintain important fidelity behaviors in human-altered habitats. However, even such species are subject to population declines in urban settings.

Fungi in the gut microbiome, collectively known as the mycobiome, are a prevalent yet neglected component of the human holobiont. A major question in the study of gut microbial communities is whether fungi exhibit eco-evolutionary patterns that are consistent with partner fidelity and long-term associations. We compared gut fungal profiles across natural populations of humans and nonhuman primates and identified significant degrees of primate-mycobiome phylosymbiosis as well as human-enriched fungal taxa. Notably, subsets of fungi are cophylogenetic and exhibit cospeciation patterns in hominids. These findings cautiously originate a new view on the eco-evolutionary potential that can shape the composition of human and primate gut mycobiomes.

Associations with symbionts within the gut lumen of hosts are particularly prone to disruption due to the constant influx of ingested food and non-symbiotic microbes, yet we know little about how partner fidelity is maintained. Here we describe for the first time the existence of a gut morphological filter capable of protecting an animal gut microbiome from disruption. The proventriculus, a valve located between the crop and midgut of insects, functions as a micro-pore filter in the Sonoran Desert turtle ant ( Cephalotes rohweri ), blocking the entry of bacteria and particles ⩾0.2 μm into the midgut and hindgut while allowing passage of dissolved nutrients. Initial establishment of symbiotic gut bacteria occurs within the first few hours after pupation via oral–rectal trophallaxis, before the proventricular filter develops. Cephalotes ants are remarkable for having maintained a consistent core gut microbiome over evolutionary time and this partner fidelity is likely enabled by the proventricular filtering mechanism. In addition, the structure and function of the cephalotine proventriculus offers a new perspective on organismal resistance to pathogenic microbes, structuring of gut microbial communities, and development and maintenance of host–microbe fidelity both during the animal life cycle and over evolutionary time.

Many interspecific interactions are shaped by coevolution. Transmission mode is thought to influence opportunities for coevolution within symbiotic interactions. Vertical transmission maintains partner fidelity, increasing opportunities for coevolution, but horizontal transmission may disrupt partner fidelity, potentially reducing opportunities for coevolution. Despite these predictions, the role of coevolution in the maintenance of horizontally transmitted symbioses is unclear. Leveraging a tractable insect–bacteria symbiosis, we tested for signatures of pairwise coevolution by assessing patterns of host–symbiont specialization. If pairwise coevolution defines the interaction, we expected to observe evidence of reciprocal specialization between hosts and their local symbionts. We found no evidence for local adaptation between sympatric lineages of Anasa tristis squash bugs and Caballeronia spp. symbionts across their native geographic range. We also found no evidence for specialization between three co-localized Anasa host species and their native Caballeronia symbionts. Our results demonstrate generalist dynamics underlie the interaction between Anasa insect hosts and their Caballeronia symbionts. We predict that selection from multiple host species may favor generalist symbiont traits through diffuse coevolution. Alternatively, selection for generalist traits may be a consequence of selection by hosts for fixed cooperative symbiont traits without coevolution.

Territorial species are unlikely to show extensive movements between breeding seasons. This is especially true for long-lived species, which often have strong pair bonding and can occupy the same territory for years. However, also in such species, individuals may face situations that can lead to a territory shift. Here, we use a comprehensive dataset documenting 40 years of breeding behavior in tawny owl (Strix aluco) – a long-lived species with high site tenacity and mate fidelity – to examine the factors affecting the decisions whether or not to move to another breeding territory and how far, as well as the fitness consequences thereof. We found that the likelihood and distance of movement in either sexes is strongly associated with a change of partner, indicating that mate loss may cause breeding dispersal. Moreover, mate change, not movement to a new territory, had negative effects on subsequent reproductive performance: individuals that changed partner were more likely to skip reproduction in the subsequent year and, in those cases they bred, they produced smaller clutches and raised fewer offspring. Our findings indicate that tawny owls change territory almost exclusively when searching for a new partner and that mate change has profound consequences on their subsequent breeding performance. Overall, our study provides evidence that in tawny owls territoriality and monogamy are associated and strongly linked to fitness, but mate fidelity may be more important than site fidelity, likely because sexes are involved in specific tasks and their cooperation ensures breeding success and, consequently, increases fitness.Significance statementBreeding dispersal, the movement of individuals between breeding sites, can entail high costs for animal fitness, especially for territorial species, which display strong site fidelity. We studied the factors associated with breeding dispersal and the consequences on breeding performances in tawny owl (Strix aluco), a highly territorial species. We found that tawny owls moved more frequently to another breeding territory when the mate died. Either sexes showed an equal probability to move, but the effect was stronger in females than in males after a mate change. Moreover, owls that changed partner showed delayed reproduction, smaller clutch and a higher probability to skip reproduction. Our findings show that in tawny owls territoriality and monogamy are associated and strongly linked to fitness, but mate fidelity may be more important than site fidelity, likely because sexes share the costs of holding the territory.

Reliable information on population size is fundamental to the management of threatened species. For wild species, mark-recapture methods are a cornerstone of abundance estimation. Here, we show the first application of the close-kin mark-recapture (CKMR) method to a terrestrial species of high conservation value; the Christmas Island flying-fox (CIFF). The CIFF is the island's last remaining native terrestrial mammal and was recently listed as critically endangered. CKMR is a powerful tool for estimating the demographic parameters central to CIFF management and circumvents the complications arising from the species’ cryptic nature, mobility, and difficult-to-survey habitat. To this end, we used genetic data from 450 CIFFs captured between 2015 and 2019 to detect kin pairs. We implemented a novel CKMR model that estimates sex-specific abundance, trend, and mortality and accommodates observations from the kin-pair distribution of male reproductive skew and mate persistence. CKMR estimated CIFF total adult female abundance to be approximately 2050 individuals (95% CI (950, 4300)). We showed that on average only 23% of the adult male population contributed to annual reproduction and strong evidence for between-year mate fidelity, an observation not previously quantified for a Pteropus species in the wild. Critically, our population estimates provide the most robust understanding of the status of this critically endangered population, informing immediate and future conservation initiatives.