Biology subjects

Arguello, J. R.

Publications and source records attributed to Arguello, J. R..

5 recordsLinked to original sources

bioRxiv2026

Evolutionary Recoding of Olfactory Sensory Neurons

Odorant receptors (Ors) are the interface between an animals nervous system and its olfactory environment. In insect genomes, the Ors are often the largest gene family, and their rapid duplications and deletions result in extensive copy-number differences between species. Because olfactory sensory neurons (OSNs) typically express only one Or (the so-called one-receptor one-neuron rule), this dynamism at the level of Or genes raises fundamental questions regarding their cellular regulation: How do new Or duplicates gain their own neuron-specific expression? Such Or-OSN changes are thought to provide a key evolutionary path for modifying olfactory perception and related behaviours, but the absence of examples of these transitions has prevented an understanding of how they occur. Using a highly duplicated Drosophila Or subfamily (the Or67a subfamily) as a model system, we discovered parallel instances of Or67a duplicates gaining new OSN expression and reconstructed their evolutionary histories. Functional work in D. suzukii, a species with two novel Or67a-expressing OSN populations, revealed that their Or67a expression has arisen in preexisting OSNs, which have lost their ancestral Ors. As a result, these neurons were recoded and acquired new olfactory identities, thereby demonstrating the diversification of an OSN repertoire without the invention of developmentally new OSN lineages.

evolutionary biology↗

bioRxiv2024

Fast and recurrent evolution of temperature preference among drosophilids

Small-bodied ectotherms are acutely vulnerable to temperature changes, but diverse thermotactic behaviours have contributed to their ability to inhabit broad climatic niches. Understanding how - and how quickly - these behaviours evolve are outstanding biological questions that are also relevant to conservation. Among insects, Drosophila melanogaster is a preeminent ectothermic model for temperate sensing and thermotaxis. However, little is known about how its temperature-related behaviours have evolved in comparison to its closely related species. We have thermo-profiled over 2400 larvae from eight closely related species of Drosophila from different thermal habitats. Consistent with local adaptation, we found substantial variation in temperature preference and fine-scale navigational behaviours amongst these species. Agent-based modelling of the larval thermotaxis circuit suggests that it is the balance between cool and warm avoidance circuits, rather than changes in temperature sensitivity, that drive differences in temperature preference. Our findings highlight the recurrent evolution of temperature-related behaviours in an experimentally tractable cross-species system.

evolutionary biology↗

bioRxiv2023

Sensory neuron population expansion enhances odour tracking through relaxed projection neuron adaptation

The evolutionary expansion of sensory neuron populations detecting important environmental cues is widespread, but functionally enigmatic. We investigated this phenomenon through comparison of homologous neural pathways of Drosophila melanogaster and its close relative Drosophila sechellia, an extreme specialist for Morinda citrifolia noni fruit. D. sechellia has evolved species-specific expansions in select, noni-detecting olfactory sensory neuron (OSN) populations, through multigenic changes. Activation and inhibition of defined proportions of neurons demonstrate that OSN population increases contribute to stronger, more persistent, noni-odor tracking behavior. These sensory neuron expansions result in increased synaptic connections with their projection neuron (PN) partners, which are conserved in number between species. Surprisingly, having more OSNs does not lead to greater odor-evoked PN sensitivity or reliability. Rather, pathways with increased sensory pooling exhibit reduced PN adaptation, likely through weakened lateral inhibition. Our work reveals an unexpected functional impact of sensory neuron expansions to explain ecologically-relevant, species-specific behavior.

neuroscience↗

bioRxiv2023

Evolution of chemosensory tissues and cells across ecologically diverse Drosophilids

Chemosensory systems display exceptional variation between species, but little is known about how the evolution of gene expression and cell types contribute to this diversity. We have generated transcriptomes for five chemosensory tissues across six ecologically diverse Drosophila species and integrated their analyses with single-cell datasets to address these questions. The evolution of chemosensory transcriptomes has been predominantly shaped by stabilizing selection, but several thousand genes have nevertheless evolved expression changes in each tissue. Phylogenetic analyses of differentially expressed genes revealed strong evidence that their expression changes have been driven by a combination of cis-regulatory and cell composition evolution. We have also found that chemosensory-related gene families have undergone pervasive expression level changes and numerous species-specific expression gains/losses. Follow-up experiments revealed several chemoreceptors that evolved novel patterns of tissue and cellular expression that likely contribute to sensory differences. Finally, analyses of the genes that are differentially expressed between sexes uncovered extensive species-specific differences. Among these rapid changes, we discovered a D. melanogaster-specific excess of male-biased gene expression in its forelegs and identified sensory and muscle cells as the primary source of this dimorphism. Together, our analyses provide new insights for understanding evolutionary changes in ecologically key tissues at both global and individual gene levels.

evolutionary biology↗

bioRxiv2021

Odorant receptor copy number change, co-expression, and positive selection establish peripheral coding differences between fly species

1.Despite numerous examples of chemoreceptor gene family expansions and contractions, how these changes relate to modifications in the neural circuitry in which they are expressed remains unclear. Drosophilas Odorant receptor (Or) family is ideal for addressing this question because a large majority of Ors are uniquely expressed in single olfactory sensory neuron (OSN) types. Between-species changes in Or copy number, therefore, may indicate diversification/reduction of OSN populations. To test this, we investigated a rapidly duplicated/deleted subfamily (named Or67a) in Drosophila melanogaster and its sister species (D. simulans, D. sechellia, and D. mauritiana). We found that the common ancestor had three Or67a paralogs that had already diverged adaptively in their odor-evoked responses. Following their speciation, two Or67a paralogs were lost independently in D. melanogaster and D. sechellia, with ongoing positive selection acting on the intact genes. Instead of the expected singular expression of each diverged Ors, the three D. simulans Or67a paralogs are co-expressed. Thus, while neuroanatomy is conserved between these species, independent selection on co-expressed receptors has contributed to species-specific peripheral coding of olfactory information. This work reveals a model of adaptive change previously not considered for olfactory evolution and raises the possibility that similar processes may be operating among the largely uninvestigated cases of Or co-expression.

evolutionary biology↗