Dataset Information

How fish eggs are preadapted for the evolution of matrotrophy.

ABSTRACT: Teleost fishes evolved livebearing via egg retention 14 times. Matrotrophy has evolved within 12 of those lineages. By contrast, squamate reptiles evolved livebearing over 115 times, but only two to four of those lineages are known to have evolved matrotrophy. Is the discrepancy between these organisms in the probability of this transition caused by differences in their eggs? We show that the eggs of oviparous species in the superorder Atherinomorpha can acquire small organic molecules from their surrounding environment against a concentration gradient via mechanisms of active transport. Uptake rates were inhibited by competing radiolabelled amino acids against unlabelled versions of themselves. Transport was non-specific as uptake rates were similar for l-leucine and its biologically uncommon enantiomer d-leucine. Eggs are also capable of transporting larger microspheres across the membrane, but transport is inhibited at temperatures below 4°C, suggesting active transport occurs via pinocytosis. Conflict theory predicts that the ability of the egg to acquire maternal resources will facilitate the embryo-parent arms race that leads to the evolution of matrotrophy following the transition to livebearing. The shelled eggs of amniotes lack such access to maternal resources when retained in the evolution of viviparity.

SUBMITTER: Morrison KR

PROVIDER: S-EPMC5719165 | biostudies-literature | 2017 Nov

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

How fish eggs are preadapted for the evolution of matrotrophy.

Morrison Keenan R KR Ngo Vyvian V Cardullo Richard A RA Reznick David N DN

Proceedings. Biological sciences 20171101 1867

Teleost fishes evolved livebearing via egg retention 14 times. Matrotrophy has evolved within 12 of those lineages. By contrast, squamate reptiles evolved livebearing over 115 times, but only two to four of those lineages are known to have evolved matrotrophy. Is the discrepancy between these organisms in the probability of this transition caused by differences in their eggs? We show that the eggs of oviparous species in the superorder Atherinomorpha can acquire small organic molecules from thei ...[more]

PMID: 29167357

Similar Datasets

Project description: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.

Project description:Domestication of finfishes is a key element toward sustainable expansion of aquaculture sector. However, huge gap in knowledge on the mechanisms of adaptability of fish to the culture environment, being the first step toward successful domestication, exists. This affects the overall production capacity which is hindered, among others, by lowered reproductive capacity of domesticated stocks, including pikeperch – a highly valued commercial freshwater fish species. Transcriptomic profiling of embryos was found to be useful tool significantly contributing into understanding domestication process in aquaculture. Up to now there is no data on transcriptomic profiling of unfertilized eggs in any fish species as well as on pikeperch, in general. Using next generation sequencing the first complex transcriptome of pikeperch have been obtained (with 40,246 unique protein-coding genes). Next, specifically designed, pikeperch-specific microarrays (Agilent technologies) were developed (with 35,343 unique probes) and transcriptomic profiling of eggs coming from wild and domesticated populations (all characterized by high quality) was performed. From among 17,543 genes found to be expressed in eggs of pikeperch 710 were found to be differentially expressed. Functional, enrichment analysis revealed that the most enriched processes represented by the set of genes identified were developmental process, regulation of phosphorylation and nervous system development. The results of the present study provides a new insight into the processes being directly involved in the successful domestication of finfishes. It can be suggested that all the identified processes were pre-determined by the maternally derived set of genes contained already in the unfertilized eggs, what has never been reported to date. In addition to that, it has been shown for the first time that among the most important processes being affected by the domestication the post translation modifications of proteins along with development of the nervous system were identified. This allows to suggest that fish behavior should be considered as a very important trait for selection for aquaculture purposes in pikeperch.

Dataset Information

How fish eggs are preadapted for the evolution of matrotrophy.

Publications

How fish eggs are preadapted for the evolution of matrotrophy.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets