Smelling in the dark: Phylogenomic insights into the chemosensory system of a subterranean beetle

Balart‐García, Pau; Cieslak, Alexandra; Escuer, Paula; Rozas, Julio; Ribera, Ignacio; Fernández, Rosa

doi:10.1111/mec.15921

Cited by 14 publications

(20 citation statements)

References 111 publications

(183 reference statements)

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“…Resulting transcriptome completeness was validated using BUSCO v.5 40 , 41 , and functional annotation was performed using TransDecoder v.5.5.0 42 and the Trinotate v.3.2.1 pipeline 38 , which employs SQLite ( http://sqlite.org/index.html ), BLAST v.2.7.1 43 , and HMMER v.3.2 ( http://hmmer.org ). Redundancy within the transcriptome assembly was reduced by retaining only the longest isoform for each Trinity gene identifier, following 10 , ensuring differential expression analysis was performed at the Trinity ‘gene’ level rather than that of isoforms. This subsetted dataset was used in downstream analyses, though we note this approach limited our ability to examine alternative splice variants.…”

Section: Methodsmentioning

confidence: 99%

“…The transition to an obligate subterranean lifestyle can cause massive shifts in an organism’s biology 1 , from the acquisition of classic troglomorphies such as the elongation of appendages for sensing in an aphotic environment 2 , to changes in lesser-studied traits including circadian rhythm 3 , 4 , reproductive biology 5 , respiration 6 , the number of larval instars 7 , 8 and chemosensation 9 , 10 . These changes have been attributed to the stark difference between subterranean and surface (hereafter epigean) habitats.…”

Section: Introductionmentioning

confidence: 99%

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Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Beasley‐Hall

Bertozzi

Bradford

et al. 2022

Sci Rep

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Subterranean habitats are generally very stable environments, and as such evolutionary transitions of organisms from surface to subterranean lifestyles may cause considerable shifts in physiology, particularly with respect to thermal tolerance. In this study we compared responses to heat shock at the molecular level in a geographically widespread, surface-dwelling water beetle to a congeneric subterranean species restricted to a single aquifer (Dytiscidae: Hydroporinae). The obligate subterranean beetle Paroster macrosturtensis is known to have a lower thermal tolerance compared to surface lineages (CTmax 38 °C cf. 42–46 °C), but the genetic basis of this physiological difference has not been characterized. We experimentally manipulated the thermal environment of 24 individuals to demonstrate that both species can mount a heat shock response at high temperatures (35 °C), as determined by comparative transcriptomics. However, genes involved in these responses differ between species and a far greater number were differentially expressed in the surface taxon, suggesting it can mount a more robust heat shock response; these data may underpin its higher thermal tolerance compared to subterranean relatives. In contrast, the subterranean species examined not only differentially expressed fewer genes in response to increasing temperatures, but also in the presence of the experimental setup employed here alone. Our results suggest P. macrosturtensis may be comparatively poorly equipped to respond to both thermally induced stress and environmental disturbances more broadly. The molecular findings presented here have conservation implications for P. macrosturtensis and contribute to a growing narrative concerning weakened thermal tolerances in obligate subterranean organisms at the molecular level.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Beasley‐Hall

Bertozzi

Bradford

et al. 2022

Sci Rep

View full text Add to dashboard Cite

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“…Resulting transcriptome completeness was validated using BUSCO v.5 (40,41), and functional annotation was performed using TransDecoder v.5.5.0 (42) and the Trinotate v.3.2.1 pipeline (38), which employs SQLite (http://sqlite.org/index.html), BLAST v.2.7.1 (43), and HMMER v.3.2 (http://hmmer.org). Redundancy within the transcriptome assembly was reduced by retaining only the longest isoform for each Trinity gene identifier, following (10), ensuring differential expression analysis was performed at the Trinity ‘gene’ level rather than that of isoforms. This subsetted dataset was used in downstream analyses to reduce redundancy, though we note this approach limited our ability to examine alternative splice variants.…”

Section: Methodsmentioning

confidence: 99%

“…Redundancy within the transcriptome assembly was reduced by retaining only the longest isoform for each Trinity gene identifier, following (10), ensuring differential expression analysis was performed at the Trinity 'gene' level rather than that of isoforms. This subsetted dataset was used in downstream analyses to reduce redundancy, though we note this approach limited our ability to examine alternative splice variants.…”

Section: Assembly Of Paroster Nigroadumbratus Reference Transcriptomementioning

confidence: 99%

“…The transition to an obligate subterranean lifestyle can cause massive shifts in an organism’s biology (1), from the acquisition of classic troglomorphies such as the elongation of appendages for sensing in an aphotic environment (2), to changes in lesser-studied traits including circadian rhythm (3,4), reproductive biology (5), respiration (6), the number of larval instars (7,8) and chemosensation (9,10). These changes have been attributed to the stark difference between subterranean and surface (hereafter epigean) habitats.…”

Section: Introductionmentioning

confidence: 99%

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Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Beasley‐Hall

Bertozzi

Bradford

et al. 2021

Preprint

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Subterranean habitats are environmentally stable with respect to temperature, humidity, and the absence of light. The transition to a subterranean lifestyle might therefore be expected to cause considerable shifts in an organism’s physiology; here, we investigate how subterranean colonisation affects thermal tolerance. Subterranean organisms might be at an increased risk of decline in the face of global temperature rises, but robust data on the fauna is lacking, particularly at the molecular level. In this study we compare the heat shock response of two species of diving beetle in the genus Paroster: one surface-dwelling (P. nigroadumbratus), the other restricted to a single aquifer (P. macrosturtensis). P. macrosturtensis has been previously established as having a lower thermal tolerance compared to surface-dwelling relatives, but the genomic basis of this difference is unknown. By sequencing transcriptomes of experimentally heat-shocked individuals and performing differential expression analysis, we demonstrate both species can mount a heat shock response at high temperatures (35C), in agreement with past survival experiments. However, the genes involved in these responses differ between species, and far greater genes are differentially expressed in the surface species, which may explain its more robust response to heat stress. In contrast, the subterranean species significantly upregulated the heat shock protein gene Hsp68 in the experimental setup under conditions it would likely encounter in nature (25C), suggesting it may be more sensitive to ambient stressors, e.g. handling. The results presented here contribute to an emerging narrative concerning weakened thermal tolerances in obligate subterranean organisms at the molecular level.

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Sniffing out morphological convergence in the turbinal complex of myrmecophagous placentals

Wright,

Martinez,

Ferreira‐Cardoso

et al. 2024

The Anatomical Record

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The length of the snout in mammals has important evolutionary consequences for the functional systems housed within the rostrum. However, whether increased snout lengths lead to expanded olfactory performance has rarely been examined. Here, we investigate inner rostral function among 10 species of myrmecophagous (ant‐ and/or termite‐eating) placental mammals and 10 closely related species. We use nondestructive computed tomography scanning methods to characterize inner rostral function based on the underlying morphology of the turbinal bones in the nasal cavity. Three approaches were chosen to address this question, including the quantification of functional turbinal surface area, the quantification of functional turbinal three‐dimensional complexity, and geometric morphometrics. By including non‐model species from several different mammalian orders, we were able to extend the discussion surrounding turbinal homologies to comparisons across mammals. Our results show no increased olfactory function in all myrmecophagous species relative to their sister taxa, which suggests that there is no trade‐off for increased olfactory capabilities in myrmecophagous species with elongated snouts. We found no evidence of convergence in turbinal morphology among all five myrmecophagous lineages. However, we found evidence of morphological convergence in the turbinals between the giant armadillo and the aardvark, suggesting a more complex interplay between the evolution of turbinal morphology and ecological correlates. While myrmecophagy alone may not be a strong enough ecological signal to overcome phylogenetic and developmental constraints, we suggest that this might be the case at the intersection of this dietary specialization with a primarily underground lifestyle where odorants may be difficult to detect.

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Smelling in the dark: Phylogenomic insights into the chemosensory system of a subterranean beetle

Abstract: Major lifestyle transitions in insects, such as the conquest of terrestrial habitats, flight or host-plant interactions, are often accompanied by dramatic shifts in their sensory systems (Almudi et al.,

Cited by 14 publications

References 111 publications

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Differential transcriptomic responses to heat stress in surface and subterranean diving beetles

Sniffing out morphological convergence in the turbinal complex of myrmecophagous placentals

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