Crab in amber reveals an early colonization of nonmarine environments during the Cretaceous

Luque, Javier; Xing, Lida; Briggs, Derek E. G.; Clark, Elizabeth G.; Duque, Alex; Hui, Jingshu; Mai, Huijuan; McKellar, Ryan C.

doi:10.1126/sciadv.abj5689

Cited by 451 publications

(29 citation statements)

References 68 publications

(99 reference statements)

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“…Whatever the process, such transmuted invaders would have been subject to selection pressures favoring the evolution of many biochemical, morphological, physiological and behavioral adaptations, including life history strategies, some probably still dependent on saline or brackish waters, that would enable eventual success in their conquest of fresh water, at least as adult semaphoronts (Havstad et al, 2015;Sharma et al, 2017;Luque et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

Strategies of invertebrate osmoregulation: an evolutionary blueprint for transmuting into fresh water from the sea

McNamara¹,

Freire²

2022

Preprint

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Early marine invertebrates like the Branchiopoda began their sojourn into dilute media some 500 million years ago in the Middle Cambrian. Others like the Mollusca, Annelida and many crustacean taxa have followed, accompanying major marine transgressions and regressions, shifting landmasses, orogenies and glaciations. In adapting to these events and new habitats such invertebrates acquired novel physiological abilities that attenuate the ion loss and water gain that constitute severe challenges to life in dilute media. Among these taxon-specific adaptations, selected from the subcellular to organismal levels of organization, are reduced body permeability and surface (S) to volume (V) ratios, lowered osmotic gradients, increased surface areas of interface epithelia, relocation of membrane proteins in ion-transporting cells and augmented transport enzyme abundance, activity and affinity. We examine adaptations in taxa that have penetrated into fresh water, revealing diversified modifications, a consequence of distinct body plans, morpho-physiological resources and occupation routes. Contingent on life history and reproductive strategy, numerous patterns of osmotic regulation have emerged, including intracellular isosmotic regulation in weak hyper-regulators and well-developed anisosmotic extracellular regulation in strong hyper-regulators, likely reflecting inertial adaptations to early life in an estuarine environment. Our analyses show that across sixty-four freshwater invertebrate species from six phyla/classes, hemolymph osmolalities decrease logarithmically with increasing S: V ratios. The arthropods have the highest osmolalities, from 300 to 650 mOsmoles/kg H2O in the Decapoda with 220 to 320 mOsmoles/kg H2O in the Insecta; osmolalities in the Annelida range from 150 to 200 mOsmoles/kg H2O, the Mollusca showing the lowest osmolalities at 40 to 120 mOsmoles/kg H2O. Overall, osmolalities reach a cut-off at ≈200 mOsmoles/kg H2O, independently of increasing S: V ratio. The ability of species with small S: V ratios to maintain large osmotic gradients is mirrored in their putatively higher Na+/K+-ATPase activities that drive ion uptake processes. Selection pressures on these morpho-physiological characteristics have led to differential osmoregulatory abilities, rendering possible the conquest of fresh water while retaining some tolerance of the ancestral medium.

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Section: Introductionmentioning

confidence: 99%

Strategies of invertebrate osmoregulation: an evolutionary blueprint for transmuting into fresh water from the sea

McNamara¹,

Freire²

2022

Preprint

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“…True crabs (Brachyura) are among the few arthropod groups that have evolved several types of compound eye, reflecting their broad range of lifestyles ( Gaten, 1998 ; Luque et al., 2019a ). However, the origins and evolution of their visual systems remain poorly constrained, the eyes of most extant families of crabs are understudied, and fossil crabs rarely preserve compound eyes and internal soft tissues ( Luque et al., 2019a , 2021 ). Here we present anatomical and ontogenetic details of the visual system of Callichimaera perplexa ( Luque et al., 2019b ), an exceptionally preserved crab from a recently discovered Cretaceous (95–90 mya) Lagerstätte of Colombia, northern South America.…”

Section: Introductionmentioning

confidence: 99%

The remarkable visual system of a Cretaceous crab

2022

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“…The colonization of land habitats by aquatic organisms is one of the most important events in the history of life on Earth [ 1 – 3 ]. Due to the chemico-physical differences between air and water (i.e., higher viscosity, thermal capacity, and lower oxygen content in water), the transition from marine to terrestrial life poses several eco-physiological challenges to living beings [ 4 ].…”

Section: Introductionmentioning

confidence: 99%

“…Although these results shed light on the role of symbiosis in the adaptation of plants to terrestrial habitats, few studies have investigated the metazoan counterpart [ 7 – 9 ]. Arthropods show very ancient and complex adaptative radiations to life on land, recurring multiple times in different geological periods [ 3 , 10 ]. They have evolved morphological, physiological and behavioural adaptations, such as cement and wax layers of the epicuticle to reduce water loss, the evolution of tracheae for air-breathing and haemoglobin/hemocyanin as a storage/respiratory pigment for oxygen transportation [ 11 ].…”

Section: Introductionmentioning

confidence: 99%

“…Brachyuran crabs are among the best examples of these adaptations, showing a wide colonization range of both marine and terrestrial habitats, with a remarkably high number of species inhabiting tidal ecosystems [ 12 , 13 ]. This adaptive flexibility, supported by paleontological evidence [ 3 , 14 , 15 ], indicates that brachyurans are still undergoing the process of terrestrial adaptation, making them a representative group for the study of this ongoing process [ 12 , 16 ].…”

Section: Introductionmentioning

confidence: 99%

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Morphological characteristics and abundance of prokaryotes associated with gills in mangrove brachyuran crabs living along a tidal gradient

et al. 2022

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Due to the chemico-physical differences between air and water, the transition from aquatic life to the land poses several challenges for animal evolution, necessitating morphological, physiological and behavioural adaptations. Microbial symbiosis is known to have played an important role in eukaryote evolution, favouring host adaptation under changing environmental conditions. We selected mangrove brachyuran crabs as a model group to investigate the prokaryotes associated with the gill of crabs dwelling at different tidal levels (subtidal, intertidal and supratidal). In these animals, the gill undergoes a high selective pressure, finely regulating multiple physiological functions during both animal submersion under and emersion from the periodical tidal events. We hypothesize that similarly to other marine animals, the gills of tidal crabs are consistently colonized by prokaryotes that may quantitatively change along the environmental gradient driven by the tides. Using electron microscopy techniques, we found a thick layer of prokaryotes over the gill surfaces of all of 12 crab species from the mangrove forests of Saudi Arabia, Kenya and South Africa. We consistently observed two distinct morphotypes (rod- and spherical-shaped), positioned horizontally and/or perpendicularly to the gill surface. The presence of replicating cells indicated that the prokaryote layer is actively growing on the gill surface. Quantitative analysis of scanning electron microscopy images and the quantification of the bacterial 16S rRNA gene by qPCR revealed a higher specific abundance of prokaryote cells per gill surface area in the subtidal species than those living in the supratidal zone. Our results revealed a correlation between prokaryote colonization of the gill surfaces and the host lifestyle. This finding indicates a possible role of prokaryote partnership within the crab gills, with potential effects on animal adaptation to different levels of the intertidal gradient present in the mangrove ecosystem.

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Crab in amber reveals an early colonization of nonmarine environments during the Cretaceous

Abstract: First Mesozoic crab in amber offers insights into the evolution of true crabs and the colonization of nonmarine environments.

Cited by 451 publications

References 68 publications

Strategies of invertebrate osmoregulation: an evolutionary blueprint for transmuting into fresh water from the sea

Strategies of invertebrate osmoregulation: an evolutionary blueprint for transmuting into fresh water from the sea

The remarkable visual system of a Cretaceous crab

Morphological characteristics and abundance of prokaryotes associated with gills in mangrove brachyuran crabs living along a tidal gradient

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