PARTHENOGENESIS or Giant Lobsters in Earth Take-Over Bid aided by Dandelion Clones

Recent publications, e.g. Underwood et al. Nature Genetics 2022, "A PARTHENOGENESIS allele from apomictic dandelion can induce egg cell division without fertilization in lettuce" have raised the ago-old questions, "why is there sex, why are there only two sexes and is sex really necessary?"

Reproduction in which two gametes unite to form a new individual is known as sexual reproduction. Sex is not essential for life and there are many examples of asexual reproduction in the plant and animal kingdoms. Apomixis is the fertilization-independent production of seeds resulting in the formation of maternally derived clonal progeny. There are other examples of clonal progeny including Dolly the Sheep and hydatidiform moles. Molar pregnancies are clonal tissues formed when an egg contains only paternal genes, rather than a set of maternal and paternal genes. Most plants reproduce via sex, but the common Dandelion makes clonal seeds via apomixis. The application of apomixis in crop species has revolutionary potential in agriculture because it would allow the propagation of hybrid genotypes, & hybrid vigour, through seeds in perpetuity.

In apomictic triploid dandelions, female meiosis is replaced by cell division without chromosomal recombination producing egg cell genetically identical to the mother plant. Genetic analysis of apomixis loci is well established in dandelion because polyploid apomictic dandelions can be used to pollinate diploid sexuals. The App haplotype (string of genes) has been conserved for between 5 to 10 million years

Apomixis in Dandelion involves skipping the two hallmarks of sexual reproduction – meiosis and fertilization. Fertilization is skipped by parthenogenesis, the formation of an embryo from an egg cell without gamete fusion. In sexual dandelion, par genes are highly expressed in pollen. In apomictic dandelion, the PAR protein represses inhibitors of embryogenesis in the egg cell, meaning that fertilization is not required. Underwood et al. mapped the dominant PARTHENOGENESIS locus in triploid apomictic Dandelion & went on to fully assemble 3 haplotypes using PacBio and Nanopore long read sequencing. They cut up the region using CAS9 mutagenesis and identified  a novel 170-amino acid protein with a C2H2 zinc finger (ZF) domain of the rare Arabidopsis K2-2 class. The striking difference between the dandelion alleles is a 1,335-bp insertion in the upstream promoter region of a miniature inverted-repeat transposable element (MITE). This insertion in the promoter  region of the gene upregulates PAR expression in eggs cells, triggering seed development without requiring fertilisation.

 

 When the PAR introduced into Lettuce it can lead to parthenogenesis. To date, parthenogenesis remains a limiting factor in dicot crops for the implementation of synthetic apomixis. Therefore, the modulation of PAR expression, and that of homologous genes in sexual crop species, could potentially contribute to the generation of apomictic crops. That could be a big advantage in agriculture wanting to grow a consistently hughly productive strain of a food crop.  However, in one case, this clonal proliferation seems to have gone of the rails: meet the clonal crayfish

This is a tale of three Crayfish:
the white clawed (Austropotamobius pallipes)

the signal (Pacifastacus leniusculus)

 

and, mostly,  the marbled (Procambarus virginalis)

With a brief visit by the slough crayfish (Procambarus fallax) - not shown.

When I was a kid in the 60’s I caught a Crayfish in the Wharfe near Appletreewick. It was about 5 inches long, the colour of limestone: the White-clawed Crayfish.  When I set it free from my bucket it swam using its tail as a paddle and quickly vanished into the rocks and plants on the river bed. 30-odd years later I found a crayfish in the Wharfe at Kettlewell.  It looked like a space-invader, being bright purple and may have been my first, and so far only, encounter with the Signal Crayfish from America, which carries “crayfish plague” to which the local Crayfish have no resistance. However a new and bizarre invader has arisen in recent years, first seen in a pet shop in Germany: the Marbled (or Texas) Crayfish. Marbled crayfish appeared first in 1995 in the German aquarium trade and is a fascinating animal. Related to the slough crayfish (Procambarus fallax) .The entire global population contains only females: a male has never been found. Marbled crayfish are the only known decapod (the group including crabs, lobsters and prawns) which can reproduce without males. Marbled crayfish reproduce by apomictic (non-meiotic) parthenogenesis. This should result in the establishment of a genetically homogeneous (clonal) population. Despite their clonality and very recent emergence, marbled crayfish are successful invaders of new territories and environments, which suggests that they are very adaptable.

Marbled crayfish are triploid (3 sets of chromosomes) with 276 chromosomes.  They have a total genome size of about 3 gigabases and encode about 24,000 genes (similar to humans). It is a triploid descendant of the sexually reproducing slough crayfish, Procambarus fallax. Because the two types cannot reproduce (although they try to mate) they can be considered distinct, reproductively isolated species. Global DNA methylation is significantly reduced in marbled crayfish, implying the involvement of molecular epigenetic mechanisms in its origination. Mitochondrial genome sequences from Heidelberg and Petshop lineages and from wild populations of Lake Moosweiher (Germany) and Madagascar were completely identical thus confirming the clonal nature of the tested populations and their single origin. The total DNA content of the marbled crayfish is 1.4x that of the slough crayfish, implying that some genome regions were lost on conversion to triploidy.

Marbled crayfish grow fast!
At day 250 after hatching, when the first females in both crayfish had reached sexual maturity, mean body weight was almost twice as large in marbled crayfish as in P. fallax females. They may also live longer. They also produce over 700 eggs compared with over 100 for P. Fallax. Therefore marbled crayfish meets all the criteria for “asexual speciation”. The morphological features and microsatellite patterns strongly suggest that marbled crayfish originated by autopolyploidisation and not by hybridisation with a closely related species.
Their high invasive potential probably results from the enhanced fitness traits discussed above and from the saved costs for the production of males, courtship, mating and meiosis.

So what?
There has been a suggestion that marbled crayfish would be a good model for salutational evolution (evolution by jumps). Also an opportunity to test theories about the evolutionary advantage of sex.
Evolutionary theory predicts short-term success of parthenogenetic lineages but their long-term extinction. The early success is usually explained by the saved costs for male production that can be used for increased growth and fecundity. The long-term extinction is explained by the accumulation of deleterious mutations (Muller's Rachet Hypothesis) and the absence of genetic variability, which impedes resistance against parasites and diseases (Red Queen Hypothesis) and adaptation to complex and changing environments (Tangled Bank Hypothesis). Read more in “Evolution of sex: The costs and benefits of sex: new insights from old asexual lineages” Roger Butlin. Discussions that are aimed at understanding the maintenance of sexual reproduction are in a bit of a quagmire owing to the many competing theories that have been proposed. Also, one of the central observations that asexual lineages are typically short lived still needs to be properly quantified. Exciting new results on ancient asexual organisms show that lineages can persist for many millions of generations without recombination. Understanding how they do so might well provide crucial new insights into the problem of sex.

The tangled bank concept states that in any given environment where there exists intense competition for space, food, and resources, diversification and genetic drift amongst species is essential for survival, as intraspecific competition can be detrimental to a population or a species.
Showing that in sufficiently complicated ecosystems, species that reproduce sexually have a greater chance of survival in the long term and, because of their greater variability, have a broader ecological valence, and are capable of utilizing broader range of available resources, highlighting the importance of sexual reproduction in order to maintain genetic diversity through DNA recombination.
Muller’s ratchet, as asexual reproduction compels genomes to be inherited as indivisible blocks, so that once the least mutated genomes in an asexual population begin to carry at least one deleterious mutation, no genomes with fewer such mutations can be expected to be found in future generations.
Red Queen Hypothesis states that coevolution could lead to situations for which the probability of extinction is relatively constant (Van Valen. 1973) this theory states that species continually need to change to keep up with the competition, and if a species would stop changing, it would lose the competition with the other species that do continue to change, and eventually could lead to extinction.

Postscript: If you are interested in the survival of the white clawed crayfish in Great Britain you can contact Surescreen Scientifics for a Forsensic Ecology kit.