Animal behavior is central in shaping the realized diel light niche

Häfker, N. Sören; Connan‐McGinty, Stacey; Hobbs, Laura; McKee, David; Cohen, Jonathan H.; Last, Kim S.

doi:10.1038/s42003-022-03472-z

Cited by 12 publications

(7 citation statements)

References 98 publications

(107 reference statements)

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“…Investigating the factors that shape phenotypic and rhythmic diversity in an integrative way will help to understand how animals adapt to specific habitats and how these factors can contribute to overall population fitness. Differences between individuals and between levels of organization are common features of biological rhythm in various clades and habitats [59,[70][71][72], and individual differences in behavioral patterns directly feed back to the experienced ("realized") environmental cycles used for entrainment [73][74][75]. It is thus important to treat biological variation not as "background noise," but as an additional aspect of biodiversity that needs to be considered in both the mechanistic and the ecological context [28,76].…”

Section: Discussionmentioning

confidence: 99%

Molecular circadian rhythms are robust in marine annelids lacking rhythmic behavior

Häfker,

Holcik,

Mat

et al. 2024

PLoS Biol

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The circadian clock controls behavior and metabolism in various organisms. However, the exact timing and strength of rhythmic phenotypes can vary significantly between individuals of the same species. This is highly relevant for rhythmically complex marine environments where organismal rhythmic diversity likely permits the occupation of different microenvironments. When investigating circadian locomotor behavior of Platynereis dumerilii, a model system for marine molecular chronobiology, we found strain-specific, high variability between individual worms. The individual patterns were maintained for several weeks. A diel head transcriptome comparison of behaviorally rhythmic versus arrhythmic wild-type worms showed that 24-h cycling of core circadian clock transcripts is identical between both behavioral phenotypes. While behaviorally arrhythmic worms showed a similar total number of cycling transcripts compared to their behaviorally rhythmic counterparts, the annotation categories of their transcripts, however, differed substantially. Consistent with their locomotor phenotype, behaviorally rhythmic worms exhibit an enrichment of cycling transcripts related to neuronal/behavioral processes. In contrast, behaviorally arrhythmic worms showed significantly increased diel cycling for metabolism- and physiology-related transcripts. The prominent role of the neuropeptide pigment-dispersing factor (PDF) in Drosophila circadian behavior prompted us to test for a possible functional involvement of Platynereis pdf. Differing from its role in Drosophila, loss of pdf impacts overall activity levels but shows only indirect effects on rhythmicity. Our results show that individuals arrhythmic in a given process can show increased rhythmicity in others. Across the Platynereis population, rhythmic phenotypes exist as a continuum, with no distinct “boundaries” between rhythmicity and arrhythmicity. We suggest that such diel rhythm breadth is an important biodiversity resource enabling the species to quickly adapt to heterogeneous or changing marine environments. In times of massive sequencing, our work also emphasizes the importance of time series and functional tests.

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Section: Discussionmentioning

confidence: 99%

Molecular circadian rhythms are robust in marine annelids lacking rhythmic behavior

Häfker,

Holcik,

Mat

et al. 2024

PLoS Biol

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“…This should result in individual-specific tolerance ranges for environmental conditions. Furthermore, patterns of behavioral rhythmicity can directly determine the environmental conditions and cycles experienced by an animal [66]. Thus, considering individual diversity in experimental planning (using multiple strains) and discussing it not as „background noise‟ but as a biological feature can advance our understanding of population- and species-level adaptability to changing environmental conditions.…”

Section: Discussionmentioning

confidence: 99%

“…This likely also affects the individual tolerance ranges for environmental conditions. Furthermore, patterns of behavioral rhythmicity can directly determine the conditions experienced by an animal 71 . Thus, a careful assessment of how many individuals one investigates, and how these are selected, is important to properly cover the individual diversity extant within a given group.…”

Section: Ecological Benefits Of Phenotypic Diversity -Beyond the Indi...mentioning

confidence: 99%

Behavioral rhythms are bad predictors of general organismal rhythmicity

Häfker

Holcik

Vadiwala

et al. 2022

Preprint

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The 24 hour day/night cycle prominently controls behavior and physiology. Most diel behaviors are under circadian clock control, but behavioral rhythmicity also exhibits significant individual diversity. Even genetically identical clones raised under the same conditions can develop distinct behavioral mannerisms. While terrestrial model systems have provided key molecular insights, the variability and molecular basis of diel rhythms in marine animals are much less investigated, although critically informative for evolutionary and ecological hypotheses. Here we investigate the phenotypic diversity of diel locomotor rhythms in the marine annelid Platynereis dumerilii. Individual-specific diel activity patterns are maintained over time, but differ strongly even between co-raised siblings. Knock-out of pigment-dispersing factor (PDF), a neuropeptide central to diel rhythmicity in Drosophila melanogaster, reveals only limited contributions of PDF to rhythmic behavioral diversity. Diel transcriptomes sampled from behaviorally rhythmic versus arrhythmic worms show no differences in circadian core clock transcript oscillations. Instead, behaviorally rhythmic worms exhibit a distinct enrichment of cycling transcripts related to behavior and neuronal differentiation, while behaviorally arrhythmic worms show an enrichment of metabolic and transport-related diel-cycling transcripts. Cycling of matrix metalloproteinases suggests that individual rhythmicity may be influenced via extracellular matrix remodeling and neuropeptide processing. Our results emphasize that organismal rhythmicity is highly complex and not necessarily properly reflected by a single read-out (like behavior or clock gene expression). We hypothesize that diversity in diel behavioral patterns allows for an adjustment to (micro)habitat conditions in the wild, thereby impacting on population fitness and adaptability to changing environmental conditions.

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“…Each of these factors independently affects organismal metabolism, with extensive literature devoted to analyses of critical oxygen partial pressure, temperature coefficients (Q 10 ), and specific dynamic action (increase in metabolic rate after consumption of food) in various marine species (Hochachka & Somero, 2002; Ikeda, 2014; Kiørboe et al., 1985; Seibel et al., 2021; Svetlichny & Hubareva, 2005; Thor, 2000). The current assumption is that an underlying circadian clock interacts with environmental changes in pressure, temperature, oxygen, and food availability, to modulate the behaviour and physiology of zooplankton across their vertical habitat (Bianchi, Stock, et al., 2013; Häfker et al., 2022; Maas et al., 2018; Piccolin et al., 2020; Tarrant et al., 2021; Teschke et al., 2011). Considering the multitude of interrelated parameters, forecasting the metabolic impact of migrators on biogeochemical cycles throughout the day becomes exceptionally challenging.…”

Section: Introductionmentioning

confidence: 99%

Diel metabolic patterns revealed by in situ transcriptome and proteome in a vertically migratory copepod

Maas,

Timmins‐Schiffman,

Tarrant

et al. 2024

Molecular Ecology

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Zooplankton undergo a diel vertical migration (DVM) which exposes them to gradients of light, temperature, oxygen, and food availability on a predictable daily schedule. Disentangling the co‐varying and potentially synergistic interactions on metabolic rates has proven difficult, despite the importance of this migration for the delivery of metabolic waste products to the distinctly different daytime (deep) and nighttime (surface) habitats. This study examines the transcriptomic and proteomic profiles of the circumglobal migratory copepod, Pleuromamma xiphias, over the diel cycle. The transcriptome showed that 96% of differentially expressed genes were upregulated during the middle of the day – the period often considered to be of lowest zooplankton activity. The changes in protein abundance were more spread out over time, peaking (42% of comparisons) in the early evening. Between 9:00 and 15:00, both the transcriptome and proteome datasets showed increased expression related to chitin synthesis and degradation. Additionally, at 09:00 and 22:00, there were increases in myosin and vitellogenin proteins, potentially linked to the stress of migration and/or reproductive investment. Based on protein abundances detected, there is an inferred switch in broad metabolic processes, shifting from electron transport system in the day to glycolysis and glycogen mobilization in the afternoon/evening. These observations provide evidence of the diel impact of DVM on transcriptomic and proteomic pathways that likely influence metabolic processes and subsequent excretion products, and clarify how this behaviour results in the direct rapid transport of waste metabolites from the surface to the deep ocean.

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Animal behavior is central in shaping the realized diel light niche

Cited by 12 publications

References 98 publications

Molecular circadian rhythms are robust in marine annelids lacking rhythmic behavior

Molecular circadian rhythms are robust in marine annelids lacking rhythmic behavior

Behavioral rhythms are bad predictors of general organismal rhythmicity

Diel metabolic patterns revealed by in situ transcriptome and proteome in a vertically migratory copepod

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