Biology subjects

Kuo, C.-Y.

Publications and source records attributed to Kuo, C.-Y..

11 recordsLinked to original sources

bioRxiv2026

Nutrient and prey-sensing signaling pathways converge on the sphingolipid methyltransferase SMT1 to regulate trap formation in a predatory fungus

The nematode trapping fungus Arthrobotrys oligospora transitions from saprophytic growth to a predatory lifestyle by forming adhesive traps in response to nutrient limitation and nematode derived cues. How nutrient availability integrates with prey sensing to control trap formation remains unclear. The presence of glucose can suppress trap formation and we found that Cre1, a conserved transcription factor that regulates the carbon catabolite repression pathway in fungi is essential for trap formation. Comparative transcriptomics and functional studies identified SMT1, which encodes a sphingolipid C9 methyltransferase, as a Cre1-dependent target that is sufficient to restore trap formation defect in the cre1 mutant. Smt1 contributes to the formation of sterol-enriched membrane domain at the tip of a growing trap hyphae and thus affects trap morphogenesis. We further discovered that the expression of SMT1 depends on both Cre1 and another transcription factor Ste12 that acts downstream of the pheromone response MAPK pathway critical for prey-sensing. These findings reveal functional crosstalk between Cre1 and Ste12 where both transcription factors are required for the expression of SMT1 and demonstrate that a predatory fungus integrates nutrient and prey-derived signals to regulate predatory lifestyle switching.

microbiology↗

bioRxiv2026

Sexual difference in defense can drive the evolution of imperfect Mllerian mimicry in the less defended sex

Mullerian mimicry is the convergent evolution of warning signals among sympatric prey driven by predator learning. Theory therefore predicts signal homogeneity both within communities and within species that participate in Mullerian mimicry. Though rare, sexual dimorphism in Mullerian species does occur, but the underlying eco-evolutionary mechanisms are still relatively unexplored. Basing on the biology of aposematic butterflies, this study uses a modeling approach to test the hypothesis that sexual difference in defense can lead to the evolution of imperfect Mullerian mimicry in the less defended females as the consequence of opposing demands to minimize the cost of automimicry while maximizing reproductive output. Additionally, both the occurrence and degree of sexual dimorphism would decrease when the less defended sex becomes more valuable for reproduction, for example when offspring sex ratio is male biased or when females can mate only once in their lifetime. Findings from this study could help explain the evolution of extreme sexual dimorphism in some Mullerian systems, in which each sex mimics different models. Moreover, through understanding this intriguing exception to the rule, we will be able to gain a more complete picture of how a multitude of selective forces might shape the diversity in prey phenotypes.

evolutionary biology↗

bioRxiv2026

A nematode-trapping fungus orchestrates polarity cues, septins, and NOX signaling for trap formation

The ability to reprogram cell morphogenesis in response to environmental cues is fundamental to microbial adaptation and survival. The nematode-trapping fungus Arthrobotrys oligospora exemplifies this plasticity by developing adhesive traps to capture nematodes. This morphological transition involves spatial reorientation of cell polarity, cytoskeletal remodeling, and cell fusion. However, the molecular mechanisms that coordinate these processes remain unclear. Using live-cell imaging, genetics, and functional assays, we demonstrated that cell polarity proteins localize to hyphal tips to direct growth, while actin and septins assemble at the curving inner rim to shape trap architecture. Conserved NADPH oxidases are induced by the presence of nematodes and are required for the recruitment of cell polarity proteins and cytoskeletal factors to promote trap cell fusion. Together, these findings reveal that polarity cues, cytoskeletal organization, and reactive oxygen species signaling are integrated to orchestrate nematode-induced trap development, establishing nematode-trapping fungi as a versatile model to study fungal cell biology.

cell biology↗

bioRxiv2024

A Sap Peptide Conserved across Flowering Plants Positively Regulates Lignin Biosynthesis, Biomass and Immunity

Signaling peptides act as hormones to deliver short- or long-distance intercellular signals to govern complex developmental processes. Identifying endogenous signaling peptides is challenging due to their low abundance and the unknown cleavage sites required for release from precursor proteins, not to mention the investigation of their evolutionary roles across species. Consequently, very few peptides were evolutionarily characterized in vivo, especially long-distance signaling peptides. Here we present current largest peptidomic datasets from six species (maize, camphor tree, tomato, rose gum, soybean and poplar), totaling 12,242 peptides, selected from all representative evolutionary clades of angiosperms, including monocots, magnoliids, rosid eudicots, and asterid eudicots. A sap peptide was found to be identical across all six species and named as ASAP (angiosperm sap peptide), emerging as the most conserved peptide family discovered thus far. ASAP rapidly induces a series of protein phosphorylation involved in a signaling cascade previously reported to regulate lignin biosynthesis, plant growth and plant immunity. Functional assays on ASAP activity demonstrated its capability on the induction of monolignol biosynthesis and lignin deposition. High-throughput phenomic analyses showed that ASAP significantly increased plant above- and below-ground biomass. In addition, ASAP treatment enhanced plant immunity and reduced the number of galls and egg masses against nematode invasion. This study provides insights into the conservation and functional significance of plant long-distance mobile signaling peptides, offering potential applications in crop improvement and disease management strategies.

plant biology↗

bioRxiv2024

Fast exploration is coupled with a less choosy but more reactive learning style in a generalist predator

The hypothesis of slow-fast syndromes predicts a correspondence between personality type and learning style; fast explorers would have a more proactive (fast but inflexible) learning style and slow explorers would be more reactive (slow but flexible) learners. Empirical evidence for this personality-cognition coupling remains inconclusive and heavily biased towards birds. Moreover, most studies did not examine the personality-cognition correlation when the cognitive task is discerning food quality, a scenario directly related to energy acquisition that underpins the evolution of slow-fast syndromes. In this study, we examined the exploration-cognition correlation in the context of avoidance learning in an opportunistic predator - the common sun skink Eutropis multifasciata. We quantified exploration tendencies of individuals in an unfamiliar environment and compared foraging behaviours when lizards associated prey colour and quality during the initial learning trials and subsequent reverse learning trials, where the prey colour-taste combinations were switched. We found that fast explorers were less choosy but more reactive foragers, whereas slow explorers exhibited the opposite learning style. Interestingly, there was no evidence for a learning speed-flexibility trade-off. Our findings are in contrast with conventional predictions and suggest that the two types of exploration-cognition coupling could be different viable responses to fast-changing environmental predictability.

animal behavior and cognition↗

bioRxiv2023

Adaptive divergence in the eyes of Heliconius butterflies likely contributes to pre- and post mating isolation

When populations experience different sensory conditions, natural selection may favor whole sensory system divergence, from the peripheral structures to the brain. We characterized the outer eye morphology of sympatric Heliconius species from different forest types, and their first-generation reciprocal hybrids to test for adaptive visual system divergence and hybrid disruption. In Panama, Heliconius cydno occurs in closed forests, whereas Heliconius melpomene resides in more open areas. Previous work has shown that, among wild individuals, H. cydno has larger eyes than H. melpomene, and there are heritable, habitat-associated differences in the visual brain structures that exceed neutral divergence expectations. Notably, hybrids have intermediate neural phenotypes, suggesting disruption. To test for similar effects in the visual periphery, we reared both species and their hybrids in common garden conditions. We confirm that H. cydno has larger eyes and provide new evidence that this is driven by selection. Hybrid eye morphology is more H. melpomene-like despite body size being intermediate, contrasting with neural trait intermediacy. Thus, eye morphology differences between H. cydno and H. melpomene are consistent with adaptive divergence, and when combined with previous neuroanatomy data, suggest hybrid visual system disruption due to mismatched patterns of intermediacy and dominance in the visual pathway.

evolutionary biology↗

bioRxiv2023

Divergent warning patterns influence male and female mating behaviours in a tropical butterfly

Traits under divergent ecological selection that also function during mating can be important in maintaining species boundaries. Few studies have considered mutual mate choice, where both males and females base mating decisions on the same trait. We investigated the contribution of visual preference to assortative mating between an aposematic butterfly Heliconius cydno and its sympatric relative H. melpomene. Wing colouration in Heliconius butterflies evolved as a warning signal but also functions as a mating cue. We predicted that both sexes of H. cydno contributed to assortative mating by exhibiting visual preference towards conspecific wing colouration. We analysed published and new data from preference experiments, in which males were presented with conspecific and H. melpomene females. We also recorded female responses and mating outcomes in choice experiments, involving conspecific males with either the original white or artificially painted red forewing bands. Both sexes of H. cydno responded more positively towards the conspecific colouration, yet male colouration did not predict mating outcomes in female choice experiments. As courtships are initiated by males in butterflies, our findings suggest that female visual preference might be of secondary importance in preventing gene flow between H. cydno and H. melpomene.

animal behavior and cognition↗

bioRxiv2023

Adaptive introgression of a visual preference gene

Visual preferences are important drivers of mate choice and sexual selection, but little is known of how they evolve at the genetic level. Here we take advantage of the diversity of bright warning patterns displayed by Heliconius butterflies, which are also used during mate choice. We show that two Heliconius species have evolved the same visual mating preferences for females with red patterns by exchanging genetic material through hybridization. Extensive behavioral experiments reveal that male preferences are associated with a genomic region of increased admixture between these two species. Variation in neural expression of regucalcin1, located within this introgressed region, correlates with visual preference across populations, and disruption of regucalcin1 with CRISPR/Cas9 impairs courtship towards conspecific females, proving a direct link between gene and behavior. Our results support a role for hybridization during behavioral evolution, and show how visually-guided behaviors contributing to adaptation and speciation are encoded within the genome.

evolutionary biology↗

bioRxiv2023

Predator learning can resolve the paradox of local warning signal diversity

Coexistence of distinct warning signals at local scales has long stood as a paradox, as selection is expected to preserve only the most common signal. So far, there has not been an explanation that is both broadly applicable and testable. This study presents a novel and generalizable resolution to this paradox (the Unforgetful Predator Hypothesis) by showing that prey displaying a rarer warning signal can persist if predators have low enough forgetting rates relative to prey generation time. In addition, inducing a high level of predator avoidance facilitates warning signal diversity when prey do not compete. In the presence of prey competition, however, warning signal diversity is more likely to occur if prey elicit intermediate levels of avoidance, such that the competitive disadvantage for individuals displaying the rare signal can be offset by predation. This hypothesis can be tested by quantifying predator avoidance and forgetting rate in laboratory and field experiments. As the level of predator avoidance is also crucial in determining the fate of rare signal in communities, I performed a meta-analysis to examine the determinants of its variation and found that higher predator avoidance can be observed in the following situations - when prey unprofitability is due to toxicity rather than mere unpalatability, when predators search widely for prey and/or prey aggregate, and when predators could differentiate between unprofitable and profitable prey using only color or pattern. In addition to resolving the paradox, these findings help inform the types of communities in which distinct warning signals can stably coexist. SignificanceCoexistence of distinct warning signals within a community represents an evolutionary paradox that still awaits a resolution that is both general and testable. I used ecologically realistic simulations to show that warning signal diversity can occur if predators have long enough memory and if prey elicit either low or moderate levels of avoidance, depending on whether they compete. A meta-analysis further shows that higher levels of predator avoidance tend to occur when unprofitable prey are highly unprofitable, when predators search widely for prey, when prey aggregate, and when prey profitability could be discerned by only color or pattern. These findings offer a testable resolution to the paradox and inform the types of communities where warning signal diversity may occur.

ecology↗

bioRxiv2022

Avoidance learning reduces intricate covariation between boldness and foraging behavior in a generalist predator

Many predators avoid unprofitable prey by learning to use visual features of the prey as reliable indicators of quality. Despite a rich literature on avoidance learning, we are still in the process of understanding how individuals might change their behavior towards unprofitable prey as information accumulates, the individual-level variation in avoidance foraging behavior, and whether learning would preserve or reduce this variation. In this study, we investigated how avoidance foraging behavior varied in a generalist lizard predator in relation to sex, population of origin, and boldness and tested the effects of learning on the variation in avoidance foraging behavior. We collected data on boldness and avoidance foraging behavior in individuals from two allopatric populations and compared variation in behavior at the beginning and end of learning experiments, in which individuals were presented with normal- and bitter-tasting prey that also differed consistently in color. We found that even though bitter prey elicited strong negative responses, lizards overall did not avoid consuming fewer such prey with learning. Instead, lizards learned to prioritize on palatable prey as they acquired more information. Our data revealed intricate covariation between boldness and avoidance foraging behavior, and the form of this covariation varied between populations, sex, and prey color. Learning overall reduced individual variation in foraging behavior, as well as the degree of covariation with boldness. Our findings highlighted the nuanced manners in which avoidance foraging behavior might manifest and suggested that learning could quickly mitigate fitness difference due to variation in behavior. Lay SummaryPredators can learn to avoid unprofitable prey using certain visual cues or signals, but avoidance foraging behavior can manifest in more subtle ways than simply "to eat or not to eat". We reported changes in foraging sequence and priority in a generalist lizard predator after learning and found that the nature of these changes depended on sex, population of origin, boldness, and prey color. We also found that learning made individuals more similar in behavior.

animal behavior and cognition↗

bioRxiv2020

Light environment influences mating behaviours during the early stages of divergence in tropical butterflies

Species divergence is facilitated when traits under divergent selection also act as mating cues. Fluctuations in sensory conditions can alter signal perception independently of adaptation to contrasting sensory environments, but how this fine scale variation affects behavioural isolation has received less attention, especially in terrestrial organisms. The warning patterns of Heliconius butterflies are under selection for aposematism and act as mating cues. Using computer vision, we extracted behavioural data from 1481 hours of video footage for 387 individuals. We show that the putative hybrid species H. heurippa and its close relative H. timareta linaresi differ in their response to divergent warning patterns, and that these differences are strengthened with increased local illuminance. Trials with live individuals reveal low-level assortative mating that are sufficiently explained by differences in visual attraction. Finally, results from hybrid butterflies are consistent with linkage between a major warning pattern gene and the corresponding behaviour, though the differences in behaviour we observe are unlikely to cause rapid reproductive isolation as predicted under a model of hybrid trait speciation. Overall, our results highlight that the role of ecological mating cues for behavioural isolation may depend on the immediate sensory conditions during which they are displayed to conspecifics.

evolutionary biology↗