Convergent evolution of an extreme dietary specialisation, the olfactory system of worm-eating rodents

Martinez, Quentin; Lebrun, Renaud; Achmadi, Anang S.; Esselstyn, Jacob A.; Evans, Alistair R.; Heaney, Lawrence R.; Miguez, Roberto Portela; Rowe, Kevin C.; Fabre, Pierre Henri

doi:10.1038/s41598-018-35827-0

Cited by 51 publications

(78 citation statements)

References 90 publications

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“…Species in different ecosystems have evolved in habitats by undergoing changes in their external and internal structure, and manifested behavioral variations to survive against various external pressures. These changes resulted in behavioral convergence despite differences across the species [27,28]. Among various environmental factors, the speci c behavioral convergence about food that is essential for survival manifests in various aspects [29,30].…”

Section: Resultsmentioning

confidence: 99%

Diversification of Leech Proboscis Structure According to Prey Ingestion Behavior

Kwak

Kim

et al. 2020

Preprint

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Background Adaptive radiation is a phenomenon in which various organs, depending on their diet and circumstance, are diversified morphologically or functionally as animals adapt to the environment. Although previous studies on changes caused by various external pressures have been well studied, the evidence for variation in invertebrates is not well known. We used freshwater leeches as an invertebrate model to observe their specific trophic niche and diversity of ingestion organ. Our results show convergent evolution according to structural changes through a representative species Alboglossiphonia sp., and the origin from common ancestor due to the remaining fluid ingestion behavior of the larval stages as a vestige.Results We identified the feeding behavior of rhynchobdellid leeches, which have the proboscis. Alboglossiphonia sp. swallows the entire prey using its proboscis, whereas proboscis leeches exhibit typical fluid-sucking behavior. We observed that proboscis of fluid-sucking leeches encompasses compartmentalized and dense muscle layers. In contrast, macrophagous leeches have relatively simple esophagus structures. To address whether the different feeding behaviors were intrinsic, we investigated the behavioral pattern and muscle arrangement in the earlier developmental stage of rhynchobdellid leeches. Interestingly, juveniles of the macrophagous leech as well as fluid-sucking leeches have the proboscis with the compartmentalized muscle layers and exhibit fluid-sucking behaviorsConclusions Animals have adapted various ways to obtain the energy needed for their survival. Diversification and evolution of ingestion methods across species further exhibit the functional morphology of the ingestion organ. However, information on ingestion behavior and internal structure is still lack and unclear, especially in invertebrate models. Our results suggest that the proboscis leeches have originated from the common fluid-sucking glossiphoniid ancestor and species diversification has led to modifications in the structure of the feeding tube. Together, leeches represent a comparative model for esophagus development according to the ingestion pattern based on diverse muscular arrangement in proboscis.

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Section: Resultsmentioning

confidence: 99%

Diversification of Leech Proboscis Structure According to Prey Ingestion Behavior

Kwak

Kim

et al. 2020

Preprint

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“…This combination leads to strong competition among closely related species sharing similar resources. Intense competition for limited resources may lead to either character displacement in resource-exploiting traits between close relatives, thereby increasing phenotypic diversity (Davies et al, 2007;Drury et al, 2018;Grant & Grant, 2006), or parallel responses, resulting in convergent phenotypes (Martinez et al, 2018;Nevo, 1979). As in other stressful habitats, the growing season at high altitudes is short, mostly limited to a 3-month summer, when pikas must build large haypiles to consume throughout the year (Dearing, 1997).…”

Section: Discussionmentioning

confidence: 99%

“…beaks, jaws, skulls) among montane organisms (Davies, Meiri, Barraclough, & Gittleman, 2007;Drury et al, 2018;Grant & Grant, 2006). Such traits play a vital role in mediating environmental interaction and often reflect adaptations to speciesspecific habitat and ecological attributes (Feijó, Patterson, & Cordeiro-Estrela, 2020;Kelley & Motani, 2015;Martinez et al, 2018;McIntosh & Cox, 2016;Rowe, Achmadi, & Esselstyn, 2016). Resourceuse phenotypic adaptations associated with restrictive habitats are well documented in subterranean (Da Silva et al, 2018;Marcy, Hadly, Sherratt, Garland, & Weisbecker, 2016;Sherratt, Gower, Klingenberg, & Wilkinson, 2014), rock-dwelling (Collar, Schulte, O'Meara, & Losos, 2010;Goodman, Miles, & Schwarzkopf, 2008;Revell, Johnson, Schulte, Kolbe, & Losos, 2007) and desert (Alhajeri & Steppan, 2018) animals.…”

Section: Introductionmentioning

confidence: 99%

Divergent adaptations in resource‐use traits explain how pikas thrive on the roof of the world

Feijó

Wen

et al. 2020

Functional Ecology

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Life in extreme environments is possible through multilevel adaptations to physical and biotic stresses. At high elevations, species face numerous challenges, besides low oxygen levels, but previous studies have focused on genetic and physiological adaptations to chronic hypoxia while overlooking other key strategies for thriving in alpine landscapes. Here, we investigate resource‐use trait adaptations to extreme elevations using pikas as a model, lagomorphs distributed up to 6,200 m and reaching maximum diversity on the Qinghai‐Tibet plateau, the highest plateau on Earth. Specifically, we assess cranial evolution in pikas using geometric morphometric and phylogenetic comparative techniques to determine whether adaptations among high‐elevation biota shown at the molecular and physiological levels also occur in resource‐use traits. We further explore the roles of two contrasting lifestyles (burrowing and rocky‐dwelling) in cranial evolution. We found that alpine species exhibit striking phenotypic specialization to distinct microhabitats. Contrary to physiological and genetic adaptive convergence, we show that the cranium has undergone adaptive divergence likely reflecting past resource competition in highlands and long‐term association with alpine landscapes. Our analyses also reveal that the evolution of burrowing lifestyle allows high‐elevation pikas to explore novel niches and boosts their phenotypic diversification. In addition to cold and hypoxia tolerance, high cranial specialization, the appearance of burrowing habits and strong niche separation explain how pikas overcome alpine stresses and flourish on the highest plateau on Earth. By contrast, when moving to spatially complex and heterogeneous vegetation zonation, pikas exhibit generalist skull forms able to exploit diverse habitats. These findings mirror previously reported intraspecific patterns in mammals, suggesting a general morphological response in resource‐exploiting traits to cope with distinct selection pressures across elevation zones. Phenotypic diversity is further constrained by rocky habitats, resulting in convergent skulls. Our study highlights that adaptations to extreme environments occur at multiple levels of organization, but can lead to distinct evolutionary paths depending on which selective forces they respond to. The evolution of burrowing behaviour represents a landmark in the evolutionary history of pikas. We further show that rocky habitats impose strong ecological pressures, leading to convergent responses in resource‐use traits, which is rarely documented in mammals.

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“…Species in different ecosystems have evolved in habitats by undergoing changes in their external and internal structure, and manifested behavioral variations to survive against various external pressures [34][35][36]. These changes resulted in behavioral convergence despite differences across the species (e.g., Rodent turbinate; Arachnid web architectures) [37,38]. Among various environmental factors, the speci c behavioral convergence about food that is essential for survival manifests in various aspects (e.g., Ultrasonic predator whale and bat) [39,40].…”

Section: Comparative Structural Morphology Of Leech Feeding Organsmentioning

confidence: 99%

Diversification of leech proboscis structure according to prey ingestion behavior

Kwak

Kim

et al. 2020

Preprint

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Background Adaptive radiation is a phenomenon in which various organs are diversified morphologically or functionally as animals adapt to environmental inputs such as diet and circumstance. Although previous studies have addressed changes caused by various external pressures, the evidence for variation in invertebrates is not well known. Leeches comprise a carnivorous or ectoparasitic group of animals that feed on a wide range of prey. They exhibit a corresponding variety of ingestion behaviors and morphological diversity of mouthparts and gut specializations. However, research on the diversity of ingestion behaviors and the internal structure of feeding organs in leeches is little known. In this study, we use histological analyses, fluorescent labeling and immunohistochemistry to reveal the detailed proboscis structure in the family Glossiphoniidae, while also suggesting the diversification of proboscises.Results We identified the feeding behavior of rhynchobdellid leeches, which have the proboscises. Alboglossiphonia sp. swallows prey whole using its proboscis, whereas other leeches exhibit typical fluid-sucking behavior. Glossiphoniid leeches exhibit fluid ingestion behavior along with clear arrangement of longitudinal muscles, circular muscles surrounding the lumen, and radial muscles, while Alboglossiphonia sp., which displays macrophagous ingestion like salifid Barbronia sp., has a partial circular muscle distribution and spacious lumen that extends to longitudinal muscle layer. To address whether the different feeding behaviors are intrinsic, we investigated the behavioral patterns and muscle arrangements in the earlier developmental stage of glossiphoniid leeches. Juvenile Glossiphoniidae including the Alboglossiphonia sp. exhibit the fluid ingestion behavior and have the proboscis with the compartmentalized muscle layers.Conclusions Genetic, morphological and behavioral differences between juvenile and adult stages of Alboglossiphonia sp. suggest their adult feeding biology has diverged from ancestral glossiphoniid leeches, while retaining developmental vestiges of the typical juvenile feeding morphology currently observed across Glossiphoniidae. This study provides the characteristics of leeches with specific ingestion behaviors, and a comparison of structural differences that serves as the first evidence of the proboscis diversification.

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Convergent evolution of an extreme dietary specialisation, the olfactory system of worm-eating rodents

Cited by 51 publications

References 90 publications

Diversification of Leech Proboscis Structure According to Prey Ingestion Behavior

Diversification of Leech Proboscis Structure According to Prey Ingestion Behavior

Divergent adaptations in resource‐use traits explain how pikas thrive on the roof of the world

Diversification of leech proboscis structure according to prey ingestion behavior

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