Spectacular alterations in the female reproductive system during the ovarian cycle and adaptations for matrotrophy in chernetid pseudoscorpions (Pseudoscorpiones: Chernetidae)
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Abstract
Pseudoscorpions are small matrotrophic chelicerates. The embryos develop in a brood
sac and feed on the nutritive fluid provided by the female. It was widely accepted
that the nutritive fluid is synthesized in the ovary. Recent studies have shown that
in
Chelifer cancroides, a representative of Cheliferidae, considered one of the most derived pseudoscorpion
families, the nutritive fluid is produced not only in the ovary but also in the oviducts.
Since evolution of adaptations for matrotrophy in pseudoscorpions is poorly known,
we aimed to verify our hypothesis that pseudoscorpions of the family Chernetidae,
closely related to Cheliferidae, share the traits of adaptations to matrotrophy in
the structure and function of the female reproductive system with
C. cancroides. We analysed the structure of the ovary and oviducts in five representatives of chernetids
with light, confocal, and transmission electron microscopy. The results confirmed
our hypothesis and provided new data which broaden our knowledge of matrotrophic pseudoscorpions.
We show that in chernetids, the ovary and oviducts undergo significant alterations
including their size, multistep hypertrophy and polyploidization of the epithelial
cells involved in secretion of the nutritive fluid, the complex secretory activity
of the epithelial cells, massive degeneration of the epithelial cells that have completed
secretion, and epithelium renewal.
Phylogenetic analyses indicate that viviparity (live-bearing reproduction) has originated independently in more than 150 vertebrate lineages, including a minimum of 115 clades of extant squamate reptiles. Other evolutionary origins of viviparity include 13 origins among bony fishes, nine among chondrichthyans, eight in amphibians, one in Paleozoic placoderms, six among extinct reptiles, and one in mammals. The origins of viviparity range geologically from the mid-Paleozoic through the Mesozoic to the Pleistocene. Substantial matrotrophy (maternal provision of nutrients to embryos during pregnancy) has arisen at least 33 times in these viviparous clades, with most (26) of these origins having occurred among fishes and amphibians. Convergent evolution in patterns of matrotrophy is widespread, as reflected by multiple independent origins of placentotrophy, histotrophy, oophagy, and embryophagy. Specializations for nutrient transfer to embryos are discontinuously distributed, reflecting the roles of phylogenetic inertia, exaptation (preadaptation), and constraint. Ancestral features that function in gas exchange and nutrition repeatedly and convergently have been co-opted for nutrient transfer, often through minor modification of their components and changes in the timing of their expression (heterochrony). Studies on functional and evolutionary morphology continue to play a central role in our attempts to understand viviparity and mechanisms of fetal nutrition.
ABSTRACT Matrotrophy, the continuous extra‐vitelline supply of nutrients from the parent to the progeny during gestation, is one of the masterpieces of nature, contributing to offspring fitness and often correlated with evolutionary diversification. The most elaborate form of matrotrophy—placentotrophy—is well known for its broad occurrence among vertebrates, but the comparative distribution and structural diversity of matrotrophic expression among invertebrates is wanting. In the first comprehensive analysis of matrotrophy across the animal kingdom, we report that regardless of the degree of expression, it is established or inferred in at least 21 of 34 animal phyla, significantly exceeding previous accounts and changing the old paradigm that these phenomena are infrequent among invertebrates. In 10 phyla, matrotrophy is represented by only one or a few species, whereas in 11 it is either not uncommon or widespread and even pervasive. Among invertebrate phyla, Platyhelminthes, Arthropoda and Bryozoa dominate, with 162, 83 and 53 partly or wholly matrotrophic families, respectively. In comparison, Chordata has more than 220 families that include or consist entirely of matrotrophic species. We analysed the distribution of reproductive patterns among and within invertebrate phyla using recently published molecular phylogenies: matrotrophy has seemingly evolved at least 140 times in all major superclades: Parazoa and Eumetazoa, Radiata and Bilateria, Protostomia and Deuterostomia, Lophotrochozoa and Ecdysozoa. In Cycliophora and some Digenea, it may have evolved twice in the same life cycle. The provisioning of developing young is associated with almost all known types of incubation chambers, with matrotrophic viviparity more widespread (20 phyla) than brooding (10 phyla). In nine phyla, both matrotrophic incubation types are present. Matrotrophy is expressed in five nutritive modes, of which histotrophy and placentotrophy are most prevalent. Oophagy, embryophagy and histophagy are rarer, plausibly evolving through heterochronous development of the embryonic mouthparts and digestive system. During gestation, matrotrophic modes can shift, intergrade, and be performed simultaneously. Invertebrate matrotrophic adaptations are less complex structurally than in chordates, but they are more diverse, being formed either by a parent, embryo, or both. In a broad and still preliminary sense, there are indications of trends or grades of evolutionarily increasing complexity of nutritive structures: formation of (i) local zones of enhanced nutritional transport (placental analogues), including specialized parent–offspring cell complexes and various appendages increasing the entire secreting and absorbing surfaces as well as the contact surface between embryo and parent, (ii) compartmentalization of the common incubatory space into more compact and ‘isolated’ chambers with presumably more effective nutritional relationships, and (iii) internal secretory (‘milk’) glands. Some placental analogues in onychophorans and arthropods mimic the simplest placental variants in vertebrates, comprising striking examples of convergent evolution acting at all levels—positional, structural and physiological.
[1
]GRID grid.8505.8, ISNI 0000 0001 1010 5103, Department of Animal Developmental Biology, Faculty of Biological Sciences, , University of Wrocław, ; Sienkiewicza 21, Wrocław, Poland
[2
]GRID grid.7634.6, ISNI 0000000109409708, Department of Zoology, Faculty of Natural Sciences, , Comenius University, ; Ilkovičova 6, Bratislava, Slovakia
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