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Houtz, J. L.

Publications and source records attributed to Houtz, J. L..

9 recordsLinked to original sources

Gut microbiota promote early-life digestive function in songbirds

The vertebrate digestive tract harbors complex microbial communities whose influences on phenotypes and fitness in non-model organisms remain poorly understood. Here, we show that colonization with gut microbiota is critical for digestive development and function in a non-model songbird, the House sparrow (Passer domesticus). We raised nestlings under sterile (axenic) conditions and compared them to nestlings reconstituted (conventionalized) with microbiota from adult sparrows. Conventionalization drove significant increases in villus length, crypt depth, goblet cell density, and mucosal thickness in the small intestine. Conventionalized nestlings also exhibited increased growth of several digestive organs and elevated circulating bile acid levels, including bacterial metabolites known to promote growth and lipid metabolism in vertebrates. These results reveal functions of songbird microbiota and establish axenic methods for non-model oviparous vertebrates.

microbiology↗

Organismal robustness and resilience influence the ability to cope with cold snaps

Coping with challenges often requires maintaining performance during poor conditions (robustness) and reestablishing normal performance following disturbance (resilience). Trade-offs between performance under normal and challenging conditions may generate variation in stress coping capacity, but there is little empirical data from wild populations. We studied robustness and resilience to temperature in tree swallows (Tachycineta bicolor) using a 39-year dataset that included >75,000 hours of behavioral data. Cold snaps had profound and sustained impacts on fitness; effects on nestlings were mediated by the behavioral robustness and resilience of parents. Parental robustness was predicted by developmental cold exposure and current endocrine state. As expected, trade-offs between peak performance and behavioral robustness influenced susceptibility. Selection on trade-offs may generate population differences in vulnerability to changing temperature regimes.

ecology↗

Divergent climate impacts despite similar response to temperature in a widespread aerial insectivore

Climate change is shifting when animals breed1,2, but it is still not clear why some populations keep pace with warming while others fall behind3,4. Differences could arise from variation in sensitivity to temperature3 or constraints on the ability to respond to temperature. Without knowing whether populations differ in sensitivity--or in their ability to act on that sensitivity--we cannot identify which are most at risk. Using 1,555 population-years from 123 populations of tree swallows (Tachycineta bicolor), we show that populations have similar sensitivity to local temperature, advancing breeding by about one day per degree of warming. However, northern populations face tighter time constraints and greater exposure to recent warming. Northern populations have advanced laying dates the most, but still experience stronger selection for earlier breeding, especially in warm years; they have also declined most in breeding abundance. These findings show that vulnerability to climate change can arise not just from different sensitivity to warming, but from when and where populations can respond effectively. By disentangling sensitivity from timing constraints, our results support a general mechanism by which even uniformly responsive species can show uneven impacts of climate change across their ranges.

ecology↗

Reproductive microbial diversity is associated with competitive phenotypes in socially polyandrous jacanas

The composition of host-associated microbial communities may reflect the overall status of the host, including physiology and reproductive success. New hypotheses suggest that reproductive microbiomes can mediate sexually selected phenotypes, which may be particularly important for species with mating systems that feature strong sexual selection. These dynamics have been particularly understudied in female animals. Using 16S rRNA sequencing, we compared the cloacal microbiome of females and males from two socially polyandrous bird species that vary in the strength of sexual selection, Jacana spinosa (Northern Jacana) and J. jacana (Wattled Jacana). We hypothesized that the strength of sexual selection would shape cloacal microbial diversity, such that the more polyandrous J. spinosa would have a more diverse microbiome, and that microbiomes would be more diverse in females than in males. If the reproductive microbiome is indicative of competitive status, we also hypothesized that cloacal microbial diversity would be associated with competitive traits, including plasma testosterone levels, body mass, or weaponry. We found a positive relationship between microbial alpha diversity and testosterone and weaponry in female J. spinosa. We found no differences in microbial alpha diversity between species or sexes, but we did find that microbial beta diversity significantly differed between species. Our results suggest that the cloacal microbiome may be a key component of the competitive phenotype in socially polyandrous jacanas, supporting the hypothesis that the interplay between sexual selection and microbial communities can shape the physiology and fitness of wild avian hosts. LAY SUMMARY- The reproductive microbiome may be a key component of the competitive phenotype - We examined cloacal microbial diversity in females and males of two Jacana species - Microbial alpha diversity is associated with testosterone and weaponry in female J. spinosa - Microbial beta diversity differed between J. spinosa and J. jacana

evolutionary biology↗

Joint effects of social interactions and environmental challenges on physiology, internal microbiome, and reproductive performance in tree swallows (Tachycineta bicolor).

The social environment that individuals experience appears to be a particularly salient mediator of stress resilience, as the nature and valence of social interactions are often related to subsequent health, physiology, microbiota, and overall stress resilience. Relatively few studies have simultaneously manipulated the social environment and ecological challenges under natural conditions. Here, we report the results of experiments in wild tree swallows (Tachycineta bicolor) in which we manipulated both ecological challenges (predator encounters and flight efficiency reduction) and social interactions (by experimental dulling of a social signal). In two experiments conducted in separate years, we reversed the order of these treatments so that females experienced either an altered social environment followed by a challenge or vice-versa. Before, during, and after treatments were applied, we tracked breeding success, morphology and physiology (mass, corticosterone, and glucose), social interactions via an RFID sensor network, cloacal microbiome diversity, and fledging success. Overall, we found that predator exposure during the nestling period reduced the likelihood of fledging and that signal manipulation sometimes altered social interactions, but little evidence that the two categories of treatment interacted with each other. We discuss the implications of our results for understanding what types of challenges and what conditions are most likely to result in interactions between the social environment and ecological challenges.

physiology↗

Developmental stage-dependent effects of perceived predation risk on physiology and fledging success of tree swallows (Tachycineta bicolor)

The risk of predation directly affects physiology, behavior, and fitness of wild birds. Social interactions with conspecifics may affect how individuals respond to stressors such as predators. Strong social connections could help individuals recover from a stressful experience; however, competitive interactions also have the potential to exacerbate stress. Few studies have investigated the interaction between environmental stressors and the social landscape in wild bird populations. Here, we experimentally simulated predation attempts on breeding female tree swallows (Tachicyneta bicolor). At the same time, we manipulated female breast plumage color, a key social signal. Simulated predation events on tree swallows negatively affected their nestlings condition, telomere lengths, and fledging success. However, the effects of experimental manipulations were timing-dependent: simulated predation during the early nestling period was more detrimental than "predation" during incubation. Contrary to our expectations, manipulation of the social environment did not affect the response of tree swallows to simulated predation. However, manipulating female plumage during the nestling period did affect nestling size, indicating an effect of the social environment on reproductive success. Our data demonstrate that transient stressors on breeding female birds can have carry-over effects on their nestlings, some of which may be long-lasting.

ecology↗

Neurogenomic landscape of social status-dependent cooperative display behavior

The neurogenomic mechanisms mediating male-male reproductive cooperative behaviors are unknown. We leveraged extensive transcriptomic and behavioral data on a neotropical bird (Pipra filicauda) that perform cooperative courtship displays to understand these mechanisms. Cooperative display is modulated by testosterone, it promotes cooperation in non-territorial birds, but suppresses cooperation in territory holders. We sought to understand the neurogenomic underpinnings of these three related traits: social status, cooperative behavior, and testosterone phenotype. To do this, we profiled gene expression in 10 brain nuclei spanning the social decision-making network (SDMN), and two key endocrine tissues that regulate social behavior. We associated gene expression with each birds behavioral and endocrine profile derived from three years of repeated measures taken from free-living birds in the Ecuadorian Amazon. We found distinct landscapes of constitutive gene expression were associated with social status, testosterone phenotype, and cooperation, reflecting the modular organization and engagement of neuroendocrine tissues. Sex-steroid and neuropeptide signaling appeared to be important in mediating status-specific relationships between testosterone and cooperation, suggesting shared regulatory mechanisms with male aggressive and sexual behaviors. We also identified differentially regulated genes involved in cellular activity and synaptic potentiation, suggesting multiple mechanisms underpin these genomic states. Finally, we identified SDMN-wide gene expression differences between territorial and floater males that could form the basis of "status-specific" neurophysiological phenotypes, potentially mediated by testosterone and growth hormone. Overall, our findings provide new, systems-level insights into the mechanisms of cooperative behavior and suggest that differences in neurogenomic state are the basis for individual differences in social behavior.

evolutionary biology↗

Investigating a trade-off between the quality of nest grown feathers and pace of development in an altricial bird.

Life history theory provides a framework for understanding how trade-offs generate negative trait associations. Among nestling birds, developmental rate, risk of predation, and lifespan covary, but some associations are only found within species while others are only observed between species. A recent comparative study suggests that allocation trade-offs may be alleviated by disinvestment in ephemeral traits, such as nest-grown feathers, that are quickly replaced. However, direct resource allocation trade-offs cannot be inferred from inter-specific trait-associations without complementary intra-specific studies. Here, we asked whether there is evidence for a within-species allocation trade-off between feather quality and developmental speed in tree swallows (Tachycineta bicolor). Consistent with the idea that ephemeral traits are deprioritized, nest-grown feathers had lower barb density than adult feathers. However, despite substantial variation in fledging age among nestlings, there was no evidence for a negative association between developmental pace and feather quality. Furthermore, accounting for differences in resource availability by considering provisioning rate and a nest predation treatment did not reveal a trade-off that was masked by variation in resources. Our results are most consistent with the idea that the inter-specific association between development and feather quality arises from adaptive specialization, rather than from a direct allocation trade-off.

ecology↗

Plumage manipulation alters the integration of social behavior, physiology, internal microbiome, and fitness.

Signals often covary with physiological and behavioral traits to form an axis of integrated phenotypic variation associated with reproductive performance. This pattern of phenotypic integration could result from intrinsic between-individual differences that are causally related to signal production, physiology, and behavior. Alternatively, signal expression itself might generate dynamic feedback between physiology, behavior, and the experienced social environment, resulting in an integrated phenotype. Here, we manipulated the plumage of female tree swallows (Tachycineta bicolor) to decouple the expression of a social signal from any pre-existing behavioral or physiological differences. We collected a time series of physiological samples, monitored social interactions with a sensor network, and tracked reproductive performance. Relative to sham controls, dulled females experienced an altered social environment; overall, these females were visited more by conspecific females and less by males. Dulled females subsequently changed their own behavior by initiating fewer interactions and increasing nestling provisioning. These differences resulted in an altered internal microbiome and glucose levels and, ultimately, dulled females produced more offspring. Moreover, dulled females produced larger clutches than control females in the year after the manipulation. Thus, signal variation alone--independent from any pre-existing differences--had a sustained causal affect on a suite of integrated traits. This finding suggests that dynamic feedback may play an important role in coordinating an integrated signaling phenotype. Our results have implications for understanding how variation in signal expression arises and is maintained and the extent to which the information encoded in signals is contingent upon their use in a social environment.

zoology↗