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1.
Proc Natl Acad Sci U S A ; 114(36): 9510-9516, 2017 09 05.
Article in English | MEDLINE | ID: mdl-28835539

ABSTRACT

We show that mucociliary membranes of animal epithelia can create fluid-mechanical microenvironments for the active recruitment of the specific microbiome of the host. In terrestrial vertebrates, these tissues are typically colonized by complex consortia and are inaccessible to observation. Such tissues can be directly examined in aquatic animals, providing valuable opportunities for the analysis of mucociliary activity in relation to bacteria recruitment. Using the squid-vibrio model system, we provide a characterization of the initial engagement of microbial symbionts along ciliated tissues. Specifically, we developed an empirical and theoretical framework to conduct a census of ciliated cell types, create structural maps, and resolve the spatiotemporal flow dynamics. Our multiscale analyses revealed two distinct, highly organized populations of cilia on the host tissues. An array of long cilia ([Formula: see text]25 [Formula: see text]m) with metachronal beat creates a flow that focuses bacteria-sized particles, at the exclusion of larger particles, into sheltered zones; there, a field of randomly beating short cilia ([Formula: see text]10 [Formula: see text]m) mixes the local fluid environment, which contains host biochemical signals known to prime symbionts for colonization. This cilia-mediated process represents a previously unrecognized mechanism for symbiont recruitment. Each mucociliary surface that recruits a microbiome such as the case described here is likely to have system-specific features. However, all mucociliary surfaces are subject to the same physical and biological constraints that are imposed by the fluid environment and the evolutionary conserved structure of cilia. As such, our study promises to provide insight into universal mechanisms that drive the recruitment of symbiotic partners.


Subject(s)
Aliivibrio fischeri/physiology , Decapodiformes/microbiology , Sense Organs/cytology , Aliivibrio fischeri/genetics , Animals , Cilia , Decapodiformes/cytology , Epithelium/ultrastructure , Microbiota , Microscopy, Video , Mucus , Sense Organs/microbiology , Symbiosis
2.
Proc Biol Sci ; 284(1857)2017 Jun 28.
Article in English | MEDLINE | ID: mdl-28637858

ABSTRACT

The social and nutritional environments during early development have the potential to affect offspring traits, but the mechanisms and molecular underpinnings of these effects remain elusive. We used Polistes fuscatus paper wasps to dissect how maternally controlled factors (vibrational signals and nourishment) interact to induce different caste developmental trajectories in female offspring, leading to worker or reproductive (gyne) traits. We established a set of caste phenotype biomarkers in P. fuscatus females, finding that gyne-destined individuals had high expression of three caste-related genes hypothesized to have roles in diapause and mitochondrial metabolism. We then experimentally manipulated maternal vibrational signals (via artificial 'antennal drumming') and nourishment levels (via restricted foraging). We found that these caste-related biomarker genes were responsive to drumming, nourishment level or their interaction. Our results provide a striking example of the potent influence of maternal and nutritional effects in influencing transcriptional activity and developmental outcomes in offspring.


Subject(s)
Larva/growth & development , Maternal Behavior , Wasps/growth & development , Animals , Female , Gene Expression Regulation , Larva/genetics , Phenotype , Reproduction , Wasps/genetics
3.
Plant Cell Environ ; 38(10): 2088-97, 2015 Oct.
Article in English | MEDLINE | ID: mdl-25754548

ABSTRACT

The elastic properties of pit membranes are reported to have important implications in understanding air-seeding phenomena in gymnosperms, and pit aspiration plays a large role in wood technological applications such as wood drying and preservative treatment. Here we present force-displacement measurements for pit membranes of circular bordered pits, collected on a mesomechanical testing system. The system consists of a quartz microprobe attached to a microforce sensor that is positioned and advanced with a micromanipulator mounted on an inverted microscope. Membrane displacement is measured from digital image analysis. Unaspirated pits from earlywood of never-dried wood of Larix and Pinus and aspirated pits from earlywood of dried wood of Larix were tested to generate force-displacement curves up to the point of membrane failure. Two failure modes were observed: rupture or tearing of the pit membrane by the microprobe tip, and the stretching of the pit membrane until the torus was forced out of the pit chamber through the pit aperture without rupture, a condition we refer to as torus prolapse.


Subject(s)
Larix/physiology , Pinus/physiology , Air , Biomechanical Phenomena , Cell Membrane/metabolism , Desiccation , Image Processing, Computer-Assisted , Larix/anatomy & histology , Models, Biological , Pinus/anatomy & histology , Rheology/instrumentation , Rheology/methods , Video Recording , Water/physiology , Wood/anatomy & histology , Wood/physiology
4.
J Exp Biol ; 214(Pt 13): 2226-36, 2011 Jul 01.
Article in English | MEDLINE | ID: mdl-21653816

ABSTRACT

Although zebra mussels (Dreissena polymorpha) initially colonized shallow habitats within the North American Great Lakes, quagga mussels (Dreissena bugensis) are becoming dominant in both shallow- and deep-water habitats. Shell morphology differs among zebra, shallow quagga and deep quagga mussels but functional consequences of such differences are unknown. We examined effects of shell morphology on locomotion for the three morphotypes on hard (typical of shallow habitats) and soft (characteristic of deep habitats) sedimentary substrates. We quantified morphology using the polar moment of inertia, a parameter used in calculating kinetic energy that describes shell area distribution and resistance to rotation. We quantified mussel locomotion by determining the ratio of rotational (K(rot)) to translational kinetic energy (K(trans)). On hard substrate, K(rot):K(trans) of deep quagga mussels was fourfold greater than for the other morphotypes, indicating greater energy expenditure in rotation relative to translation. On soft substrate, K(rot):K(trans) of deep quagga mussels was approximately one-third of that on hard substrate, indicating lower energy expenditure in rotation on soft substrate. Overall, our study demonstrates that shell morphology correlates with differences in locomotion (i.e. K(rot):K(trans)) among morphotypes. Although deep quagga mussels were similar to zebra and shallow quagga mussels in terms of energy expenditure on sedimentary substrate, their morphology was energetically maladaptive for linear movement on hard substrate. As quagga mussels can possess two distinct morphotypes (i.e. shallow and deep morphs), they might more effectively utilize a broader range of substrates than zebra mussels, potentially enhancing their ability to colonize a wider range of habitats.


Subject(s)
Bivalvia/physiology , Locomotion , Algorithms , Animal Structures/anatomy & histology , Animals , Biomechanical Phenomena , Ecosystem , Fresh Water , Great Lakes Region , Kinetics , Models, Biological , Models, Statistical , Movement , Species Specificity
5.
Curr Biol ; 21(3): 231-5, 2011 Feb 08.
Article in English | MEDLINE | ID: mdl-21256023

ABSTRACT

Understanding the proximate mechanisms of caste development in eusocial taxa can reveal how social species evolved from solitary ancestors. In Polistes wasps, the current paradigm holds that differential amounts of nutrition during the larval stage cause the divergence of worker and gyne (potential queen) castes. But nutrition level alone cannot explain how the first few females to be produced in a colony develop rapidly yet have small body sizes and worker phenotypes. Here, we provide evidence that a mechanical signal biases caste toward a worker phenotype. In Polistes fuscatus, the signal takes the form of antennal drumming (AD), wherein a female trills her antennae synchronously on the rims of nest cells while feeding prey-liquid to larvae. The frequency of AD occurrence is high early in the colony cycle, when larvae destined to become workers are being reared, and low late in the cycle, when gynes are being reared. Subjecting gyne-destined brood to simulated AD-frequency vibrations caused them to emerge as adults with reduced fat stores, a worker trait. This suggests that AD influences the larval developmental trajectory by inhibiting a physiological element that is necessary to trigger diapause, a gyne trait.


Subject(s)
Behavior, Animal , Hierarchy, Social , Wasps/growth & development , Animals , Body Fat Distribution , Female , Larva/growth & development , Physical Stimulation , Wasps/anatomy & histology , Wasps/physiology
6.
J Exp Biol ; 213(Pt 15): 2602-9, 2010 Aug 01.
Article in English | MEDLINE | ID: mdl-20639421

ABSTRACT

The invasive zebra mussel (Dreissena polymorpha) has quickly colonized shallow-water habitats in the North American Great Lakes since the 1980s but the quagga mussel (Dreissena bugensis) is becoming dominant in both shallow and deep-water habitats. While quagga mussel shell morphology differs between shallow and deep habitats, functional causes and consequences of such difference are unknown. We examined whether quagga mussel shell morphology could be induced by three environmental variables through developmental plasticity. We predicted that shallow-water conditions (high temperature, food quantity, water motion) would yield a morphotype typical of wild quagga mussels from shallow habitats, while deep-water conditions (low temperature, food quantity, water motion) would yield a morphotype present in deep habitats. We tested this prediction by examining shell morphology and growth rate of quagga mussels collected from shallow and deep habitats and reared under common-garden treatments that manipulated the three variables. Shell morphology was quantified using the polar moment of inertia. Of the variables tested, temperature had the greatest effect on shell morphology. Higher temperature (approximately 18-20 degrees C) yielded a morphotype typical of wild shallow mussels regardless of the levels of food quantity or water motion. In contrast, lower temperature (approximately 6-8 degrees C) yielded a morphotype approaching that of wild deep mussels. If shell morphology has functional consequences in particular habitats, a plastic response might confer quagga mussels with a greater ability than zebra mussels to colonize a wider range of habitats within the Great Lakes.


Subject(s)
Animal Structures/anatomy & histology , Animal Structures/growth & development , Dreissena/anatomy & histology , Dreissena/growth & development , Ecosystem , Fresh Water , Animals , Body Weight , Great Lakes Region
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