Kleptogenesis

Lorraine Boissoneault, "Genetic Mystery: The all-female salamanders of the Great Lakes", Great Lakes Now 11/2/2021:

Looking at them, you wouldn’t guess that the unisexual Ambystoma salamanders are any different than the other members of what was once considered their group.

These interlopers were previously grouped with five other mole salamander species: the tiger salamanders with yellow stripes; the blue-spotted salamander, marked as its name suggests; the brownish smallmouth salamander and Jefferson salamander; and the pale streamside salamander. All five species have lithe, wet bodies, bulbous eyes, and cutely smiling faces.

What sets the mysterious unnamed Ambystoma species apart is something that can only be seen by looking at their genetics. They’re an all-female lineage—and they steal genetic material from all five other species of salamander in their region, a feat that would seem impossible if not for the fact that these lady salamanders have been around for more than 5 million years.

"We often get asked, ‘What is the species name for these organisms?’ And the answer is that we don’t have one because they don’t play by the rules of what we would typically call a species," said Rob Denton, professor of biology at Marian University.

Scientists aren’t quite sure of how these salamanders manage to combine so much divergent genetic material without their offspring having any ill effects. The reproductive process is a little more straightforward. Male salamanders of all these species will leave packets of sperm around the wetlands in the spring. The unisexual females seek out the sperm, absorb it into their own genitals, and this stimulates reproduction. The females can continue seeking out sperm packets and incorporating all that genetic material into their offspring, or they can make simple clones.

As for the females who belong to one of the distinct species, whether it’s the blue-spotted salamanders or the Jefferson salamanders, they can’t mate with males of different species.

Because the process is thought to be totally unique to this line of unisexual salamanders, it was given its own name: kleptogenesis, in which females steal genetic material.

According to Barbara Mable, "Sex in the postgenomic era.Trends in ecology & evolution 2007:

In combining genomic in situ hybridization (GISH), microsatellite genotyping and mitochondrial DNA sequencing with >20 years of data on genomic composition, Bogart et al.  have coined the term ‘kleptogenesis’ to describe the reproductive mode used by these salamanders. They propose that the unisexuals arose through an ancient hybridization event between an A. laterale male and an A. barboui-like female. The most intriguing implication of these studies is that the A. barbouri nuclear genome has been completely replaced, while leaving its mitochondrial genome behind. The current genomic composition of the hybrids has resulted from genome swapping and whole-genome additions as the unisexuals moved into sympatry with other sexual species from which they were able to ‘steal’ sperm (kleptos = to steal).

The cited source for the coinage is Bogart, James P., Ke Bi, Jinzong Fu, Daniel WA Noble, and John Niedzwiecki. "Unisexual salamanders (genus Ambystoma) present a new reproductive mode for eukaryotes.Genome 2007:

To persist, unisexual and asexual eukaryotes must have reproductive modes that circumvent normal bisexual reproduction. Parthenogenesis, gynogenesis, and hybridogenesis are the modes that have generally been ascribed to various unisexuals. Unisexual Ambystoma are abundant around the Great Lakes region of North America, and have variously been described as having all 3 reproductive modes. Diploid and polyploid unisexuals have nuclear genomes that combine the haploid genomes of 2 to 4 distinct sexual species, but the mtDNA is unlike any of those 4 species and is similar to another species, Ambystoma barbouri. To obtain better resolution of the reproductive mode used by unisexual Ambystoma and to explore the relationship of A. barbouri to the unisexuals, we sequenced the mitochondrial control and highly variable intergenic spacer region of 48 ambystomatids, which included 28 unisexuals, representatives of the 4 sexual species and A. barbouri. The unisexuals have similar sequences over most of their range, and form a close sister group to A. barbouri, with an estimated time of divergence of 2.4-3.9 million years ago. Individuals from the Lake Erie Islands (Kelleys, Pelee, North Bass) have a haplotype that demonstrates an isolation event. We examined highly variable microsatellite loci, and found that the genetic makeup of the unisexuals is highly variable and that unisexual individuals share microsatellite alleles with sexual individuals within populations. Although many progeny from the same female had the same genotype for 5 microsatellite DNA loci, there was no indication that any particular genome is consistently inherited in a clonal fashion in a population. The reproductive mode used by unisexual Ambystoma appears to be unique; we suggest kleptogenesis as a new unisexual reproductive mode that is used by these salamanders.

The male salamanders of various Ambystoma species "leave packets of sperm around the wetlands in the spring", so why call the female/unisexual Ambystomas' actions "stealing" rather than "gathering" or "harvesting"? Maybe it's because there's a well-known Greek compound element klepto- for thief, used in English words like keptomania and kleptocrat, whereas English derivatives of e.g. ἀγείρω "of things, collect, gather" appear not to exist. Or maybe what these salamanders is doing is perceived as immoral as well as unusual?

The Great Lakes Now article is the most recent of several example where this word, and the concepts behind it, have appeared in the mass media:

Rachel Feltman, "How a female-only line of salamanders ‘steals’ genes from unsuspecting males", Popular Science 6/14/2017
Misti Crane, "Unisexual salamander evolution: A long, strange trip", OSU News 7/25/2018
Katie Garrett & Daniel Peterschmidt, "The Unisexuals: A Story of Salamanders and Sex", Science Friday 5/22/2019

[h/t Robert Shackleton]