Parallel morphological evolution and habitat-dependent sexual dimorphism in cave- vs. surface populations of the Asellus aquaticus (Crustacea: Isopoda: Asellidae) species complex

Studying parallel evolution (repeated, independent evolution of similar phenotypes in similar environments) is a powerful tool to understand environment-dependent selective forces. Surface-dwelling species that repeatedly and independently colonized caves provide unique models for such studies. The primarily surface-dwelling Asellus aquaticus species complex is a good candidate to carry out such research, because it colonized several caves in Europe. By comparing 17 functional morphological traits between six cave and nine surface populations of the A. aquaticus species complex, we investigated population divergence in morphology and sexual dimorphism. We found habitat-dependent population divergence in 10 out of 17 traits, likely reflecting habitat-driven changes in selection acting on sensory systems, feeding, grooming, and antipredator mechanisms. Sexual dimorphism was present in 15 traits, explained by sexual selection acting on male traits important in male-male agonistic behavior or mate guarding and fecundity selection acting on female traits affecting offspring number and nursing. In eight traits, the degree of sexual dimorphism was habitat dependent. We conclude that cave-related morphological changes are highly trait- and function-specific and that the strength of sexual/fecundity selection strongly differs between cave and surface habitats. The considerable population variation within habitat type warrants further studies to reveal cave-specific adaptations besides the parallel patterns

Environmental filtering and convergent evolution determine the ecological specialisation of subterranean spiders

Ecological specialization is an important mechanism enhancing species coexistence within a given community. Yet, unravelling the effect of multiple selective evolutionary and ecological factors leading the process of specialization remains a key challenge in ecology. Subterranean habitats provide highly replicated experimental arenas in which to disentangle the relative contribution of evolutionary history (convergent evolution vs. character displacement) and ecological setting (environmental filtering vs. competitive exclusion) in driving community assembly. We tested alternative hypotheses about the emergence of ecological specialization using the radiation of a lineage of sheet‐weaver cave‐dwelling spiders as model system. We observed that at the local scale, a differential specialization to cave microhabitats generally parallels moderate levels of morphological similarity and close phylogenetic relatedness among species. Conversely, geographic distance contributed little in explaining microhabitat occupation, possibly mirroring a limited role of competitive exclusion. Yet, compared to non‐coexisting species, co‐occurring species adapted to different microhabitats showed lower morphological niche overlap (i.e. higher dissimilarity) and deeper genetic distance. The framework here developed suggests that in the subterranean domain, habitat specialization is primarily driven by environmental filtering, secondarily by convergent evolution, and only marginally by character displacement or competitive exclusion. This pattern results in the establishment of replicated communities across geographical space, composed by ecologically equivalent species. Such process of community assembly well explains the numerous adaptive radiations observed in subterranean habitats, an eco‐evolutionary pattern well documented in oceanic islands or mountain summit communities

Towards evidence-based conservation of subterranean ecosystems

Subterranean ecosystems are among the most widespread environments on Earth, yet we still have poor knowledge of their biodiversity. To raise awareness of subterranean ecosystems, the essential services they provide, and their unique conservation challenges, 2021 and 2022 were designated International Years of Caves and Karst. As these ecosystems have traditionally been overlooked in global conservation agendas and multilateral agreements, a quantitative assessment of solution-based approaches to safeguard subterranean biota and associated habitats is timely. This assessment allows researchers and practitioners to understand the progress made and research needs in subterranean ecology and management. We conducted a systematic review of peer-reviewed and grey literature focused on subterranean ecosystems globally (terrestrial, freshwater, and saltwater systems), to quantify the available evidence-base for the effectiveness of conservation interventions. We selected 708 publications from the years 1964 to 2021 that discussed, recommended, or implemented 1,954 conservation interventions in subterranean ecosystems. We noted a steep increase in the number of studies from the 2000s while, surprisingly, the proportion of studies quantifying the impact of conservation interventions has steadily and significantly decreased in recent years. The effectiveness of 31% of conservation interventions has been tested statistically. We further highlight that 64% of the reported research occurred in the Palearctic and Nearctic biogeographic regions. Assessments of the effectiveness of conservation interventions were heavily biased towards indirect measures (monitoring and risk assessment), a limited sample of organisms (mostly arthropods and bats), and more accessible systems (terrestrial caves). Our results indicate that most conservation science in the field of subterranean biology does not apply a rigorous quantitative approach, resulting in sparse evidence for the effectiveness of interventions. This raises the important question of how to make conservation efforts more feasible to implement, cost-effective, and long-lasting. Although there is no single remedy, we propose a suite of potential solutions to focus our efforts better towards increasing statistical testing and stress the importance of standardising study reporting to facilitate meta-analytical exercises. We also provide a database summarising the available literature, which will help to build quantitative knowledge about interventions likely to yield the greatest impacts depending upon the subterranean species and habitats of interest. We view this as a starting point to shift away from the widespread tendency of recommending conservation interventions based on anecdotal and expert-based information rather than scientific evidence, without quantitatively testing their effectiveness.Peer reviewe

A conservation roadmap for the subterranean biome

The 15th UN Convention on Biological Diversity (CBD) (COP15) will be held in Kunming, China in October 2021. Historically, CBDs and other multilateral treaties have either alluded to or entirely overlooked the subterranean biome. A multilateral effort to robustly examine, monitor, and incorporate the subterranean biome into future conservation targets will enable the CBD to further improve the ecological effectiveness of protected areas by including groundwater resources, subterranean ecosystem services, and the profoundly endemic subsurface biodiversity. To this end, we proffer a conservation roadmap that embodies five conceptual areas: (1) science gaps and data management needs; (2) anthropogenic stressors; (3) socioeconomic analysis and conflict resolution; (4) environmental education; and (5) national policies and multilateral agreements.Peer reviewe

Coevolution of life history traits and morphology in female subterranean amphipods

Subterranean species show a distinct morphology, yet the adaptive significance of some traits, like body size and shape, is poorly understood and cannot be explained solely by distinct environmental conditions (darkness, less food). We predicted that in females some morphological changes may have co‐evolved with life history traits, and that co‐evolving life history traits provide at least part of the explanation for evolutionary changes of morphology. Using museum material we tested this prediction on the subterranean amphipod genus Niphargus . We studied six species found in springs and eight species found in cave lakes. We treated them as two ecologically distinct groups, and the major ecological differences between them were the availability of nutrients and the water currents. Cave species were found to be larger and stouter (as inferred from the shape of coxal plates, which are part of the marsupium), they had larger eggs and lower reproductive effort per brood, whereas the egg number and brood volume if corrected for the body size were not different. Using phylogenetic independent contrasts, we found a positive correlation between body shape and egg volume, a positive correlation between body size and egg volume, and a negative correlation between body size and reproductive effort per brood. We tentatively conclude that evolutions of morphology and life histories are functionally connected and that co‐evolving traits contribute to overall selective regime

The Vertical Extent of Groundwater Metazoans: An Ecological and Evolutionary Perspective

We investigated the upper and lower vertical limits of the distribution of inhabitants of the most abundant freshwater habitat—groundwater. Distribution in photic habitats is limited by competition, predation, and risks of exposure to ultraviolet radiation. Nonetheless, a number of eyeless, depigmented subterranean species occur in twilight habitats, taking advantage of the higher food resources available and modulating their distribution by photophobic behavior. We argue that the upper boundary is an interesting system in the study of classic ecological and evolutionary questions. The lower boundary of the distribution of groundwater species (approximately 2000—4000 meters) is likely controlled by physicochemical parameters, including temperature, pressure, and oxygen. The lower boundary warrants further research, and it is one of the most poorly explored areas of the biosphere

The importance of naming cryptic species and the conservation of endemic subterranean amphipods

Molecular taxonomy often uncovers cryptic species, reminding us that taxonomic incompleteness is even more severe than previous thought. The importance of cryptic species for conservation is poorly understood. Although some cryptic species may be seriously threatened or otherwise important, they are rarely included in conservation programs as most of them remain undescribed. We analysed the importance of cryptic species in conservation by scrutinizing the South European cryptic complex of the subterranean amphipod Niphargus stygius sensu lato. Using uni- and multilocus delineation methods we show that it consists of 15 parapatric and sympatric species, which we describe using molecular diagnoses. The new species are not mere “taxonomic inflation” as they originate from several distinct branches within the genus and coexist with no evidence of lineage sharing. They are as evolutionarily distinct as average nominal species of the same genus. Ignoring these cryptic species will underestimate the number of subterranean endemics in Slovenia by 12 and in Croatia by four species, although alpha diversity of single caves remains unchanged. The new taxonomy renders national Red Lists largely obsolete, as they list mostly large-ranged species but omit critically endangered single-site endemics. Formal naming of cryptic species is critical for them to be included in conservation policies and faunal listings

SupplementaryMaterial_DataMatrices

The file contains list of communities with coordinates, a table of species occurrences, morphometric data, list of species used in phylogenetic analysis, details of molecular analyses, a table of species co-occurrence records, a table of pairwise Euclidean distances and a table of pairwise Patristic distances

Data from: Niches within a niche: ecological differentiation of subterranean amphipods across Europe’s interstitial waters

Species that successfully colonized subterranean environments are subject to two opposing selection processes. Stringent abiotic factors select for convergent adaptations, such as loss of eyes and pigments, while interspecific competition drives between-species divergence. Subterranean species can resolve opposing selection by adaptation to physically different microhabitats. Yet, species frequently co-occur in physically homogeneous subterranean habitats, like interstitial. These co-occurrences in such a narrow ecological context can be explained either by equalizing mechanisms, in which neither of the co-occurring species has a competitive advantage, or by more complex niche models that include species’ differentiation along a trophic niche axis. We tested these hypotheses using the amphipod genus Niphargus. We analysed Europe-wide co-occurrence records of Niphargus species from interstitial habitats, split into six independent large-scale regions. Firstly, we addressed whether species’ pairwise co-occurrences are random using a probabilistic model. Secondly, we tested whether species cluster into distinct functional-morphological groups and whether ecologically or phylogenetically distinct species are more likely to co-occur. We found that 68 % of species co-occurrences were not different from random expectation, indicating that most species had access to most sites within each region. The remaining 32 % co-occurred either significantly more or less often than expected by chance. Cluster analysis of functional morphological characters showed that interstitial species belong to two feeding types, micro- and macrofeeders, likely representing two peaks of the interstitial adaptive landscape, and hinting that niche divergence, as a mechanism allowing coexistence, is favoured. Finally, we found that the number of co-occurrences increases with increasing differentiation of functional morphology, but not phylogenetic differences. We conclude that ecological differentiation may be important in shaping such interstitial communities