Cave amphipods reveal co‐variation between morphology and trophic niche in a low‐productivity environment

Premate, Ester; Borko, Špela; Delić, Teo; Malard, Florian; Simon, Laurent

doi:10.1111/fwb.13797

Cited by 29 publications

(19 citation statements)

References 77 publications

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“…The observed general morphological similarity might either support true morphological crypsis or indicate that all studied individuals belong to the same species. As it was already presented for other amphipods, morphological traits accurately re ect occupied trophic niche [73][74][75][76] and therefore morphological similarity likely indicates the same ecological niche and similar use of available resources [82,83]. Since multiple species competing for the same resources are unlikely to coexist in the same (micro)habitat (according to the competitive exclusion principle), morphological evidence supports the hypothesis that co-occurring MOTUs of E. sicilianus in fact represent the same species.…”

Section: Discussionmentioning

confidence: 55%

See 1 more Smart Citation

COI is not enough: integrative taxonomy reveals striking overestimation of species diversity in a Mediterranean freshwater amphipod

Hupało

Copilaş‐Ciocianu²,

Leese

et al. 2022

Preprint

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BackgroundThe emergence of DNA taxonomy sparked a paradigm shift in biodiversity assessments and revealed the existence of many morphologically cryptic species in all ecosystems worldwide. For animals, DNA-based assessments of species diversity usually rely on the mitochondrial cytochrome c oxidase subunit I (COI) gene. However, an increasing number of studies report patterns of mito-nuclear discordance originating for example from shared ancestral polymorphisms or introgression, leading to an over- or underestimation of true species diversity. Therefore, reports of mitochondrial lineages should be verified by other methods. Freshwater amphipods are ideal model organisms since putative cryptic species have been reported in many of the nominal taxa. In this study, we investigated the species status of the numerous mitochondrial molecular operational taxonomic units (MOTUs) found within the Mediterranean freshwater amphipod Echinogammarus sicilianus on Sicily. For validation, we used an integrative taxonomic approach combining DNA barcoding with behavioural data, detailed morphometrics and genome-wide double digest restriction site-associated DNA sequencing (ddRAD-seq). Results Within a relatively small sampling area (approx. 200 km2), we detected 12 divergent COI MOTUs, with genetic distances ranging from 1.8% to 20.3% and a mean distance of 11%. At 17 of the 25 sampling sites up to six MOTUs occurred in syntopy. The four most common MOTUs were analysed with high resolution morphometric data (49 measurements per specimen), but we found no clear evidence of morphological differentiation among them. We also observed a high level of MOTU intermixing (38%) in precopulatory pairs. Similarly, ten of the mitochondrial MOTUs were not supported by the genome-wide ddRAD-seq data. However, for the two remaining mitochondrial MOTUs found at sites outside of the main river stretch, ddRAD-seq and COI data were congruent, indicating that those MOTUs might indeed represent cryptic species. Conclusions Our study on the amphipod E. sicilianus reveals another prominent example of mito-nuclear discordance indicating that species delimitation based solely on mitochondrial markers can significantly overestimate species diversity. The study highlights that integrative taxonomy approaches are important for validating species status, especially in hyperdiverse species complexes, where many mitochondrial MOTUs occur in close proximity or even syntopy.

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Section: Discussionmentioning

confidence: 55%

“…We examined morphological differentiation by measuring 49 traits that re ect diet, locomotion and reproduction [73][74][75][76](see Tab. S5).…”

Section: Morphologymentioning

confidence: 99%

COI is not enough: integrative taxonomy reveals striking overestimation of species diversity in a Mediterranean freshwater amphipod

Hupało

Copilaş‐Ciocianu²,

Leese

et al. 2022

Preprint

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“…The low survival rates of the surface species might be linked to both competition and predation by the stygobiont one, and suggests the need for a further control condition for the epigean species in future studies. Niphargus amphipods are often considered generalist species feeding on detritus (Luštrik et al 2011;Tachet 2010), but opportunistic predatory behaviours can be more frequent than usually reported (Ercoli et al 2019;Fišer et al 2010), and predator species have been recently recognised (Premate et al 2021). However, we never observed direct predation by Niphargus on E. stammeri.…”

Section: Discussionmentioning

confidence: 99%

Behavioural drivers of ecotone exploitation: activity of groundwater animals in spring

Manenti

Galbiati

Lapadula

et al. 2023

Behav Ecol Sociobiol

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Border habitats such as interfaces and ecotones are promising research targets being likely areas of high species richness and genetic and phenotypic diversity. Springs are intriguing habitats exploited by both subterranean and surface species. For subterranean species, springs can provide higher trophic resources but can be risky in terms of predation and UV radiation, while for surface species, springs can be safer but less productive environments. We coupled field surveys and laboratory experiments to understand how predation risk and physical constraints, like light occurrence, affect spring exploitation by both a subterranean (Niphargus thuringius) and a surface crustacean amphipod species (Echinogammarus stammeri). From March to May 2021, we surveyed multiple springs and evaluated the activity (both during day and night) of the amphipods and of their predators. Furthermore, in a subterranean laboratory, we reared 80 N. thuringius and 80 E. stammeri under safe and risky conditions with both constant darkness and diel light variation assessing their activity and survival. Risky conditions were represented by the occurrence of meso-predators alone or coupled with the presence of a top predator. In the field, N. thuringius activity was negatively related to the density of predators, while laboratory experiments revealed a main role played by light treatments and night period. E. stammeri activity in the field was higher close to surface while in laboratory conditions decreased during time. In laboratory conditions, predation risk negatively affected survival of both amphipods. Our findings reveal that physical constraints play a key role in affecting the exploitation of ecotones and can mediate antipredator responses, thus providing selective pressures for the exploitation of border environments. Significance statement Understanding environmental pressures acting on ecotones is a key point to verify if new adaptations may occur at the border between two distinct habitats. Using both field and laboratory approaches, we show that, in springs, the behaviour of subterranean invertebrates is affected by surface physical constraints which can mediate the effects of predation risk. Behavioural strategies to avoid predation, such as nocturnal activity, may promote spring ecotone exploitation by groundwater animals, such as amphipod crustaceans.

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“…We examined morphological differentiation by measuring 49 traits that reflect diet, locomotion and reproduction (Copilaș‐Ciocianu et al., 2021; Fišer et al., 2013; Kralj‐Fišer et al., 2020; Premate et al., 2021) (Table S5). A complete description of landmarks and function of the examined traits is provided in Copilaș‐Ciocianu et al.…”

Section: Methodsmentioning

confidence: 99%

Morphology, nuclear SNPs and mate selection reveal that COI barcoding overestimates species diversity in a Mediterranean freshwater amphipod by an order of magnitude

et al. 2022

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DNA sequence information has revealed many morphologically cryptic species worldwide. For animals, DNA‐based assessments of species diversity usually rely on the mitochondrial cytochrome c oxidase subunit I (COI) gene. However, a growing amount of evidence indicate that mitochondrial markers alone can lead to misleading species diversity estimates due to mito‐nuclear discordance. Therefore, reports of putative species based solely on mitochondrial DNA should be verified by other methods, especially in cases where COI sequences are identical for different morphospecies or where divergence within the same morphospecies is high. Freshwater amphipods are particularly interesting in this context because numerous putative cryptic species have been reported. Here, we investigated the species status of the numerous mitochondrial molecular operational taxonomic units (MOTUs) found within Echinogammarus sicilianus. We used an integrative approach combining DNA barcoding with mate selection observations, detailed morphometrics and genome‐wide double digest restriction site‐associated DNA sequencing (ddRAD‐seq). Within a relatively small sampling area, we detected twelve COI MOTUs (divergence = 1.8–20.3%), co‐occurring in syntopy at two‐thirds of the investigated sites. We found that pair formation was random and there was extensive nuclear gene flow among the ten MOTUs co‐occurring within the same river stretch. The four most common MOTUs were also indistinguishable with respect to functional morphology. Therefore, the evidence best fits the hypothesis of a single, yet genetically diverse, species within the main river system. The only two MOTUs sampled outside the focal area were genetically distinct at the nuclear level and may represent distinct species. Our study reveals that COI‐based species delimitation can significantly overestimate species diversity, highlighting the importance of integrative taxonomy for species validation, especially in hyperdiverse complexes with syntopically occurring mitochondrial MOTUs.

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Cave amphipods reveal co‐variation between morphology and trophic niche in a low‐productivity environment

Cited by 29 publications

References 77 publications

COI is not enough: integrative taxonomy reveals striking overestimation of species diversity in a Mediterranean freshwater amphipod

COI is not enough: integrative taxonomy reveals striking overestimation of species diversity in a Mediterranean freshwater amphipod

Behavioural drivers of ecotone exploitation: activity of groundwater animals in spring

Morphology, nuclear SNPs and mate selection reveal that COI barcoding overestimates species diversity in a Mediterranean freshwater amphipod by an order of magnitude

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