Matrotrophy and placentation in invertebrates: a new paradigm

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 mimi...

Placental structures and their association with matrotrophy and superfetation in poeciliid fishes

“…For each characteristic, the models are listed from best to worst fit Several studies have used the matrotrophy index as an indicator of the degree of placentation (e.g., Ostrovsky et al, 2016;Pollux et al, 2014;Reznick et al, 2002). These two models used phylogenetic generalized least squares, assuming a Brownian motion evolutionary model (PGLS-BM) and an ordinary least squares model, which assumes that characteristics adapt immediately to their environments.…”

The genetics of egg retention and fertilization success inDrosophila: One step closer to understanding the transition from facultative to obligate viviparity

“…Viviparity has evolved from oviparity many times independently in animals–it has originated in over 150 vertebrate‐ (Blackburn ) and over 140 invertebrate lineages (Ostrovsky et al. ); even within Dipteran species alone, the proposed number of independent origins exceeds 60 (Meier et al. ).…”

“…Recently, however, the pervasiveness of such patterns in invertebrates has gained attention as well (reviewed in Ostrovsky et al. ), with even more diverse matrotrophic adaptations being present in invertebrates than in vertebrate species.…”

“…Viviparity has evolved from oviparity many times independently in animals-it has originated in over 150 vertebrate- (Blackburn 2015) and over 140 invertebrate lineages (Ostrovsky et al 2016); even within Dipteran species alone, the proposed number of independent origins exceeds 60 (Meier et al 1999). Intriguingly, some reptiles have both viviparous and oviparous populations, implying that viviparity can originate at subspecific levels (Qualls et al 1995;Blackburn 2015;Braz et al 2016).…”

Phylogenetically Widespread Polyembryony in Cyclostome Bryozoans and the Protracted Asynchronous Release of Clonal Brood-Mates

“…This represents the division of labour between zooidal polymorphs within the cyclostome colony, allowing the sustained extra-embryonic nutrition of both primary and cloned embryos. Polyembryony in cyclostomes (via matrotrophy [46]) may therefore be characterised by maternal control of reproductive output, in terms of brood number and larval output, in response to resource availability. This scenario contrasts with polyembryony in nine-banded armadillos, which produce a single brood of a predetermined size (four embryos), possibly to circumvent constraints imposed by the single egg implantation site present in the uterus [45].…”