Search bioRxiv⌕ Search

Biology subjects

Pujic, Z.

Publications and source records attributed to Pujic, Z..

6 recordsLinked to original sources

A coordinated morphogenetic program drives rapid body plan transformation in a sponge

Across the animal kingdom, metamorphosis transforms a free-swimming larva into a morphologically distinct juvenile, yet how conserved cellular processes are spatiotemporally coordinated to execute this rapid body plan switch remains poorly understood. Using the marine sponge Amphimedon queenslandica -- a member of one of the earliest-diverging animal phyletic lineages -- we characterise the cellular and morphogenetic events of the first six hours of metamorphosis. We show that metamorphosis proceeds through a tightly ordered sequence of events orchestrated by a stereotypic wave of epithelial infoldings that propagates from the basal to the apical pole within the first hour post-settlement. This wave acts as a morphogenetic pacemaker, spatially and temporally inducing subsequent cellular transitions, which include coordinated mucus secretion, cilia resorption, epithelial-mesenchymal transition (EMT), mesenchymal-epithelial transition (MET), transdifferentiation and targeted programmed cell death. Lineage tracing further reveals the stepwise transformation of larval cells at metamorphosis, with labelled epithelial flask cells transdifferentiating into internal archaeocyte stem cells via a transitory amoeboid cell state associated with EMT. These findings demonstrate that rapid metamorphosis comprises a spatially pre-patterned, stepwise program, and provide a cellular framework for understanding body plan transformations with broad implications for the evolution of metazoan metamorphosis.

developmental biology↗

Light-entrained chromatin priming poises rapid metamorphosis in a marine sponge

The most widespread animal life cycle includes a planktonic larval stage that is environmentally induced to settle and rapidly metamorphose into a benthic juvenile. Although this transition is critical for survival, how planetary cues such as light interact with local ecological signals to prepare the genome for such rapid reprogramming remains poorly understood. Here, using the sponge Amphimedon queenslandica, we integrate time-resolved transcriptomic and chromatin accessibility profiling across larval competence, settlement, and the first hours of metamorphosis. We show that diminishing light at sunset is associated with extensive chromatin remodelling in swimming larvae prior to settlement, despite relatively modest changes in gene expression. Upon environmental induction by a coralline alga, metamorphosis is accompanied by the rapid and transient activation of a large suite of deeply conserved transcription factors, including AP-1/bZIP family members, whose binding motifs are enriched in newly accessible regulatory regions near differentially expressed genes. Larvae prevented from experiencing sunset by constant light fail to settle and instead adopt an alternative transcriptional and chromatin state characterised by widespread loss of accessibility and repression of competence-associated transcription factors, including the circadian regulator CLOCK and other bHLH-PAS factors. These observations support a model in which light-entrained transcriptional activity establishes an anticipatory, permissive chromatin landscape that enables immediate and coordinated transcriptional reprogramming upon environmental induction. We propose that such chromatin priming may represent a broadly deployed regulatory strategy underlying the speed and robustness of metamorphosis in biphasic animal life cycles.

developmental biology↗

Behavioral adaptation to changing energy constraints via altered frequency of movement selection

Animal behavior is strongly constrained by energy consumption. A natural manipulation which provides insight into this constraint is development, where an animal must adapt its movement to a changing energy landscape as its body grows. Unlike many other animals, for fish it is relatively easy to estimate the energy consumed by their movements via fluid mechanics. Here we simulated the fluid mechanics of >100,000 experimentally-recorded movement bouts from larval zebrafish across different ages and fluid conditions as they hunted Paramecia. We find that these fish adapt to their changing relationship with the fluid environment as they grow by adjusting the frequency with which they select different types of movements, so that more expensive movements are chosen less often. This strategy was preserved when fish were raised in an unnaturally viscous environment. This work suggests a general principle by which animals could minimize energy consumption in the face of changing energy costs over development.

animal behavior and cognition↗

fmr1 mutation interacts with sensory experience to alter the early development of behavior and sensory coding in zebrafish

While Autism Spectrum Disorders (ASDs) are developmental in origin little is known about how they affect the early development of behavior and sensory coding, or how this is modulated by the sensory environment. The most common inherited form of autism is Fragile X syndrome, caused by a mutation in FMR1. Here we show that zebrafish fmr1-/- mutant larvae raised in a naturalistic visual environment display early deficits in hunting behavior, tectal map development, tectal network properties and decoding of spatial stimuli. However when given a choice they preferred an environment with reduced visual stimulation, and rearing them in this environment improved these metrics. Older fmr1-/- fish showed differences in social behavior, spending more time observing a conspecific, but responding more slowly to social cues. Together these results help reveal how fmr1-/- changes the early development of vertebrate brain function, and how manipulating the environment could potentially help reduce these changes.

neuroscience↗

Behavioral signatures of a developing neural code

During early life neural codes must develop to appropriately transform sensory inputs into behavioral outputs. Here we demonstrate a direct link between the maturity of neural coding in the visual brain and developmental changes in visually-guided behavior. In zebrafish larvae we show that visually-driven hunting behavior improves from 4 to 15 days post-fertilization, becoming faster and more accurate. During the same period population activity in the optic tectum refines, leading to improved decoding and information transmission of spatial position, particularly in the representation of the frontal visual field. Remarkably, individual differences in decoding can predict each fishs hunting success. Together these results show how the neural codes required to subserve a natural behavior emerge during development.

neuroscience↗

Model-based decoupling of evoked and spontaneous neural activity in calcium imaging data

The pattern of neural activity evoked by a stimulus can be substantially affected by ongoing spontaneous activity. Separating these two types of activity is particularly important for calcium imaging data given the slow temporal dynamics of calcium indicators. Here we present a statistical model that decouples stimulus-driven activity from low dimensional spontaneous activity in this case. The model identifies hidden factors giving rise to spontaneous activity while jointly estimating stimulus tuning properties that account for the confounding effects that these factors introduce. By applying our model to data from zebrafish optic tectum and mouse visual cortex, we obtain quantitative measurements of the extent that neurons in each case are driven by evoked activity, spontaneous activity, and their interaction. This broadly applicable model brings new insight into population-level neural activity in single trials without averaging away potentially important information encoded in spontaneous activity.

neuroscience↗