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Parthenogenesis: Birth of a New Lineage or Reproductive Accident?

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Casper J Van der Kooi at University of Groningen
Casper J Van der Kooi
Tanja Schwander at University of Lausanne
Tanja Schwander
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Parthenogenesis - the ability to produce offspring from unfertilized eggs - is widespread among invertebrates and now increasingly found in normally sexual vertebrates. Are these cases reproductive errors or could they be a first step in the emergence of new parthenogenetic lineages? Copyright © 2015 Elsevier Ltd. All rights reserved.
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Parthenogenesis: Birth of a New Lineage or
Reproductive Accident?
Casper J. van der Kooi and Tanja Schwander
University of Lausanne, Department of Ecology and Evolution, Le Biophore, CH – 1015 Lausanne, Switzerland
Correspondence: Casper.vanderKooi@unil.ch (C.J.v.d.K.), Tanja.Schwander@unil.ch (T.S.)
http://dx.doi.org/10.1016/j.cub.2015.06.055
Parthenogenesis — the ability to produce offspring from unfertilized eggs — is widespread among
invertebrates and now increasingly found in normally sexual vertebrates. Are these cases reproductive
errors or could they be a first step in the emergence of new parthenogenetic lineages?
The phenomenon of virgin birth has long
fascinated scientists and laymen alike.
The first account of parthenogenesis in
the literature is the prophecy of Jesus
Christ’s birth in Isaiah 7:14: ‘‘Therefore the
Lord himself will give you a sign: The virgin
will conceive and give birth to a son, and
will call him Immanuel’’. This reference to
parthenogenesis is unusual in two ways:
first, it is the only account of ‘natural
parthenogenesis’ in a mammal. Mammals
are believed to be completely unable to
reproduce via parthenogenesis because
of a number of developmental and genetic
constraints [1]. Second, while the
‘‘Blessed Virgin Mary’’ might have been
able to conceive a daughter via
parthenogenesis, the conception of a
son is highly unlikely. As male sex in
humans is determined by genes on the
Y chromosome, Mary, as a woman,
could not have transmitted any
Y chromosomes to her offspring. In
contrast to humans, parthenogenetic
production of sons is expected in species
with other types of sex determination.
For example, in birds, some reptiles and
Current Biology 25, R654–R676, August 3, 2015 ª2015 Elsevier Ltd All rights reserved R659
Current Biology
Dispatches
butterflies, females are the heterogametic
sex: they carry two differentiated sex
chromosomes (Z and W) while males
are homogametic (ZZ). This sex
determination system can result in the
virgin birth of sons if parthenogenesis is
automictic [2], whereby oocytes undergo
a normal meiosis that results in four
haploid products (one egg cell and three
polar bodies). Under sexual reproduction,
the polar bodies would degenerate and
the egg cell would fuse with a sperm
to generate a diploid zygote. Under
automictic parthenogenesis, diploidy is
restored via the fusion of the egg cell
and one of the polar bodies [2].As
in self-fertilization or mating with
relatives, automictic parthenogenesis
can cause an increase in homozygosity,
including homozygosity at the sex
chromosome. Hence ZW females can
parthenogenetically produce ZZ sons
and ZW daughters (WW individuals are
generally not viable). Thus, automictic
parthenogenesis is the mechanism
underlying the occasional production
of sons and daughters well known for
many species of bagworm moths [3]
and recently described in some reptile
species, including Komodo dragons [4]
and snakes [5].
While male-producing parthenogenesis
is rare, female-producingparthenogenesis
is widespread among animals and
mostly obligate (Figure 1), with many
documented cases in species-rich
invertebrate groups such as insects,
nematodes and crustaceans, and with
only few examples in vertebrates [2].A
recent paper by Fields et al. [6] in Current
Biology documents a new case of
female-producing parthenogenesis in
a critically endangered ray species,
the sawfish Pristis pectinata.Pristis
species — like all sawfish — are
characterized by their elongated flat nose
lined with teeth. P. pectinata occurs in
coastal areas of the western Atlantic sea,
mostly in bay areas around Florida. A
microsatellite-based genetic screen of
190 individuals in a wild population
revealed seven females that were most
likely produced via parthenogenesis.
Parthenogenetic ancestry was deduced
because the seven females were
homozygous at all or almost all screened
loci [6]. Mating between relatives can also
result in homozygosity, but individuals in
the screened population were not related
to each other. Furthermore, mating
between close relatives is unlikely given
the ecology of the species, leaving
parthenogenesis as the most likely
explanation [6].
Are these parthenogenetically
produced sawfish females rare
‘accidents’, or could they be indicative
of a unique case of adaptive, facultative
parthenogenesis in a vertebrate?
Facultative parthenogenesis, where
an individual female can produce
offspring either sexually or
parthenogenetically (Figure 1), is
exceedingly rare among animals. A
much more widespread phenomenon
is accidental parthenogenesis — also
called spontaneous parthenogenesis,
or tychoparthenogenesis [7]: the hatching
of a very small proportion of unfertilized
eggs in a normal, sexual species.
For example, in different species of
Drosophila, observed rates of accidental
parthenogenesis in natural populations
range from one egg in 100,000 to one in a
million successfully developing into an
adult [8]. These hatching rates are orders
of magnitude lower than for facultative
parthenogenesis, where the majority of
unfertilized eggs hatch. However, without
systematic screens for hatching success
of eggs laid by virgin females, accidental
and facultative parthenogenesis can be
difficult to distinguish. Widely popularized
examples of rare parthenogenesis in
vertebrates are typically interpreted as
facultative parthenogenesis [9], including
reports of parthenogenesis in sharks
[10,11], snakes [5] and Komodo dragons
[4], producing offspring while kept
solitarily in captivity. Given the current
evidence, these examples are, however,
most likely cases of accidental rather than
facultative parthenogenesis, mimicking
the high incidence of accidental
parthenogenesis among invertebrates.
Distinguishing whether the sawfish
females are a case of facultative,
accidental, or obligate parthenogenesis
would require additional studies, ideally
involving breeding experiments. Although
such experiments might be difficult to
conduct with P. pectinata because of
its ecological requirements, they could
generate interesting insights into the
evolution of parthenogenesis. For
example, because of its great inefficiency,
accidental parthenogenesis [7,8] is
generally not adaptive (Figure 1). An
exception might be situations where
sexual females fail to find a mate. Stalker
[12] predicted that in marginal populations
or other situations where mates are
limited even inefficient accidental
parthenogenesis could be adaptive and
thus selectively favored. This prediction
is supported by evidence from natural
populations of Drosophila vinegar flies
and stick insects. In these species,
accidental parthenogenesis rates are
especially high in low-density populations
where large fractions of adult females
remain unmated [13,14]. Thus, via the
accumulation of gradual changes,
accidental parthenogenesis might be a
stepping-stone to ‘true’ parthenogenesis
and give rise to new facultative or obligate
parthenogenetic lineages.
Sexual
reproduction
Accidental
parthenogenesis
Obligate
parthenogenesis
Facultative
parthenogenesis
Sexual
reproduction
Current Biology
Female may reproduce via
sex and/or parthenogenesis
with
Figure 1. The efficiency of parthenogenesis varies widely.
Accidental parthenogenesis refers to the very rare hatching of unfertilized eggs in sexual populations,
often due to reproductive errors, that can generate male offspring in species with female heterogame ty.
Given the very low hatching success, accidental parthenogenesis is often not adaptive. Under
facultative parthenogenesis a female may reproduce via sex and/or parthenogenesis; hence this
reproductive mode combines the advantages of sex and parthenogene sis. Under obligate
parthenogenesis, females cannot reproduce sexually at all, even if mated to males of sexual lineages.
Populations consisting solely of obligate parthenogens are characterized by the virtual absence of
males. However, many species feature mixed reproduction, with some females reproducing sexually
and others via obligate parthenogenesis. These species are characterized by sex ratios ranging from
50:50 to strongly female-biased.
R660 Current Biology 25, R654–R676, August 3, 2015 ª2015 Elsevier Ltd All rights reserved
Current Biology
Dispatches
So, could accidental parthenogenesis
in humans ever give rise to a new
parthenogenetic lineage? Probably
not, as the developmental and genetic
constraints in humans and other
mammals would most likely prevent the
emergence of adaptive parthenogenesis
in natural populations [1]. As it turns out,
even the most famous speculation about
parthenogenesis, Jesus Christ’s birth,
owes its existence not to a miracle but to a
human error during the translation of
Isaiah 7:14 from Hebrew to Greek: The
Hebrew word almah can refer to a young
woman of marriageable age, whether
married or not [15]. The ‘young woman’
became a ‘virgin’ in the gospel according
to Matthew, where almah was translated
as the Greek parthenos.
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Binocular Vision: Joining Up the Eyes
Andrew T. Smith
Department of Psychology, Royal Holloway, University of London, Egham, Surrey TW20 0EX, UK
Correspondence: a.t.smith@rhul.ac.uk
http://dx.doi.org/10.1016/j.cub.2015.06.013
To provide a unitary view of the external world, signals from the two eyes must be combined: a new study
pinpoints the location in the human brain where the requisite combination occurs.
A fundamental feature of human vision is
that, despite having two eyes, we
normally see only one representation of
the world around us. This phenomenon,
imaginatively termed cyclopean
perception by the late Bela Julesz [1],
requires a seamless combination of two
completely separate neural signals and
imposes on the brain a substantial
computational burden that a cyclops
would be spared. There are, however,
a number of benefits to having two
eyes that collectively outweigh the
computational cost. Perhaps the most
obvious, although not necessarily the
evolutionary driver, is insurance against
loss of an eye. Another is that it permits a
wider field of view (only modestly wider in
humans but much wider in horses, sheep
and many other mammals). The most
studied benefit is that having two eyes
permits stereoscopic vision: the
construction of accurate estimates of the
distances of nearby objects based on
subtle differences between the two retinal
images. These benefits depend on the
replacement of two representations of the
world by a single, cyclopean
representation. Where in the brain does
this happen? It might be expected that a
harmonious coalition of left and right
would be constructed at the very first
processing stage at which both signals
are present in proximity: the thalamus;
however, it has long been known that this
is not the case and that the answer is
‘‘somewhere in the visual cortex’’. In this
issue of Current Biology, Barendregt et al.
[2] present evidence from functional
magnetic resonance imaging (fMRI) that
the transformation occurs between the
primary visual cortex, known as V1, and
the second visual area, V2.
Whether a given neuron is responsive to
light stimulation in either eye or is driven
only by one eye has been addressed in
many neurophysiological studies, starting
with the pioneering work of Nobel Prize
winners Hubel and Wiesel, who found that
the primary visual cortex of macaques
contains a mixed bag of cells, some
Current Biology 25, R654–R676, August 3, 2015 ª2015 Elsevier Ltd All rights reserved R661
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Dispatches
... In the parthenogenetic biotype, females produce unreduced eggs with the same genomic composition as somatic cells, and these unreduced eggs spontaneously develop into individuals without fertilization (Lutes et al., 2010). Consistent parthenogenesis is widespread in invertebrates and Squamata of vertebrates (Avise, 2015;van der Kooi and Schwander, 2015). In aquaculture animals, marbled crayfish (Procambarus virginalis) has been detected to reproduce via parthenogenesis (Scholtz et al., 2003). ...
... Unisexual reproduction without meiosis and meiotic recombination cannot purge deleterious mutations (Muller's ratchet) (Muller, 1964) and create genetic diversity (Red queen hypothesis) (Van Valen, 1973), which is considered an evolutionarily dead-end (Avise, 2015). However, some unisexual lineages have exhibited wide ecological distribution and outlived their predicted time of extinction, such as bdelloid rotifers (Mark Welch and Meselson, 2000), amoebae (Maciver, 2016), salamanders (Bi and Bogart, 2010;Bogart, 2019), Amazon molly (Loewe and Lamatsch, 2008;Warren et al., 2018), and gibel carp (Liu et al., 2017b;. ...
Sex determination mechanisms and sex control approaches in aquaculture animals
Article
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  • May 2022
Aquaculture is one of the most efficient modes of animal protein production and plays an important role in global food security. Aquaculture animals exhibit extraordinarily diverse sexual phenotypes and underlying mechanisms, providing an ideal system to perform sex determination research, one of the important areas in life science. Moreover, sex is also one of the most valuable traits because sexual dimorphism in growth, size, and other economic characteristics commonly exist in aquaculture animals. Here, we synthesize current knowledge of sex determination mechanisms, sex chromosome evolution, reproduction strategies, and sexual dimorphism, and also review several approaches for sex control in aquaculture animals, including artificial gynogenesis, application of sex-specific or sex chromosome-linked markers, artificial sex reversal, as well as gene editing. We anticipate that better understanding of sex determination mechanisms and innovation of sex control approaches will facilitate sustainable development of aquaculture.
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... Tychoparthenogenesis is characterized by a low hatching rate and a weak survival probability of the offspring (Little et al., 2017). It is typically considered as a dead-end accidental phenomenon in species adapted to sexual reproduction, although it may also correspond to an intermediate state in the evolution toward asexuality (van der Kooi and Schwander, 2015). ...
... The question remains as to whether the phenomenon is accidental or an ongoing evolutionary process due to its adaptive benefit (van der Kooi and Schwander, 2015). Studying the occurrence of parthenogenesis among Ephemeroptera, Liegeois et al. (2021) suggested that asexual reproduction was selectively advantageous in many species from this insect order despite its associated low hatching success. ...
Spontaneous parthenogenesis in the parasitoid wasp Cotesia typhae: low frequency anomaly or evolving process?
Preprint
  • Dec 2021
A bstract Hymenopterans are haplodiploids and unlike most other Arthropods they do not possess sexual chromosomes. Sex determination typically happens via the ploidy of individuals: haploids become males and diploids become females. Arrhenotoky is believed to be the ancestral reproduction mode in Hymenopterans, with haploid males produced parthenogenetically, and diploid females produced sexually. However, a number of transitions towards thelytoky (diploid females produced parthenogenetically) have appeared in Hymenopterans, and in most cases populations or species are either totally arrhenotokous or totally thelytokous. Here we present the case of Cotesia typhae (Fernandez-Triana), a Braconidae that produces parthenogenetic females at a low frequency. The phenotyping of two laboratory strains and one natural population showed that this frequency is variable, and that this rare thelytokous phenomenon also happens in the wild. Moreover, mated females from one of the laboratory strains produce a few parthenogenetic daughters among a majority of sexual daughters. The analysis of daughters of heterozygous virgin females allowed us to show that a mechanism similar to automixis with central fusion is very likely at play in C. typhae . This mechanism allows some parts of the genome to remain heterozygous, especially at the chromosomes’ centromeres, which can be advantageous depending on the sex determination system involved. Lastly, in most species, the origin of thelytoky is either bacterial or genetic, and an antibiotic treatment as well as PCR experiments did not demonstrate a bacterial cause in C. typhae . The unusual case of low parthenogenetic frequency described in this species constitutes another example of the fascinating diversity of sex determination systems in Arthropods.
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... Furthermore, squamates represent the only vertebrates with obligate or true (sperm-independent) parthenogenesis [12,62,63], which can also be characterized by occasional backcrossing with one or more parental or related species [64]. Nevertheless, unisexual reproduction is not restricted to polyploid squamates, and facultative parthenogenesis is generally associated with diploid species [65,66]. ...
Evolutionary and Genomic Diversity of True Polyploidy in Tetrapods
Article
Full-text available
  • Mar 2023
True polyploid organisms have more than two chromosome sets in their somatic and germline cells. Polyploidy is a major evolutionary force and has played a significant role in the early genomic evolution of plants, different invertebrate taxa, chordates, and teleosts. However, the contribution of polyploidy to the generation of new genomic, ecological, and species diversity in tetrapods has traditionally been underestimated. Indeed, polyploidy represents an important pathway of genomic evolution, occurring in most higher-taxa tetrapods and displaying a variety of different forms, genomic configurations, and biological implications. Herein, we report and discuss the available information on the different origins and evolutionary and ecological significance of true polyploidy in tetrapods. Among the main tetrapod lineages, modern amphibians have an unparalleled diversity of polyploids and, until recently, they were considered to be the only vertebrates with closely related diploid and polyploid bisexual species or populations. In reptiles, polyploidy was thought to be restricted to squamates and associated with parthenogenesis. In birds and mammals, true polyploidy has generally been considered absent (non-tolerated). These views are being changed due to an accumulation of new data, and the impact as well as the different evolutionary and ecological implications of polyploidy in tetrapods, deserve a broader evaluation.
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... Accidental parthenogenesis, often incorrectly referred to as tychoparthenogenesis, has been observed in several vertebrates. Accidental parthenogenesis involves the parthenogenetic development of a very small portion of unfertilised eggs in a sexually reproducing species (van der Kooi and Schwander, 2015). ...
Genetic and cellular characterisation of parthenogenesis in the brown alga Ectocarpus sp.
Thesis
  • Dec 2018
Although sexual reproduction predominates in eukaryotes, several hundred lineages have undergone the transition from sexuality to asexuality. Transitions between sexual and asexual reproduction are believed to have important evolutionary and ecological consequences, yet the molecular, genetic, and cytological foundations of such transitions remain elusive. One type of asexual reproduction is parthenogenesis, i.e., the development of an adult organism directly from gametes in the absence of fertilisation. Although many eukaryotes are capable of reproducing by parthenogenesis, we know very little about its genetic basis, and the evolutionary causes and consequences of transitions to asexuality are poorly understood. The brown algae are a group of multicellular eukaryotes, that show an extraordinary diversity of types of life cycle, sexual systems, modes of reproduction, and they provide excellent models to look at the origins, evolution and mechanisms underlying parthenogenesis. In this thesis, we have used a wide array of genomic and cell biology tools available for the model brown alga Ectocarpus to identify and characterize loci involved in parthenogenesis, shedding light on the causes and consequences of parthenogenesis at the organism level. Our results highlight the key role of the sex chromosome as a major regulator of asexual reproduction, together with two autosomal loci. Importantly, we identify several negative effects of parthenogenesis on male fitness, but also different fitness effects between parthenogenesis and life cycle generations, supporting the idea that parthenogenesis may be under both sexual selection and generation/ploidally-antagonistic selection (Chapter 2). Zygotic growth was significantly affected by the parthenogenetic capacity of the male parent and the putative role of mitochondrial inheritance patterns on the fitness of sporophytes was also investigated (Chapter 2 and 3). This work revealed an unusual transmission pattern of mitochondria specifically in Ectocarpus species 7 (Chapter 3). Finally, the QTL analysis (Chapter 2) required the construction of a genetic map for Ectocarpus siliculosus and a comparison with Ectocarpus species 7 genetic map (reference genome sequenced in 2010) showed that the synteny was highly conserved between the two species (Chapter 4). By investigating parthenogenesis in a multicellular organism that has independently evolved from plants and animals, the work presented in this thesis has helped to assess the diversity of evolutionary mechanisms that lead to parthenogenesis.
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... These concerns are further amplified by the findings that FP may be heritable 5,6 , which could lead to greater incidence of this phenomenon in small populations as a result of inbreeding 3 . Despite advances that recent studies have made towards understanding FP in vertebrates 9 , the fundamental questions of: (i) resolving which automictic mechanism(s) underlie FP, and (ii) how FP impacts individual-level genetic diversity on a genome-scale, remain unresolved. ...
Genome wide data implicate terminal fusion automixis in king cobra facultative parthenogenesis
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Full-text available
  • Mar 2021
Facultative parthenogenesis (FP) is widespread in the animal kingdom. In vertebrates it was first described in poultry nearly 70 years ago, and since then reports involving other taxa have increased considerably. In the last two decades, numerous reports of FP have emerged in elasmobranch fishes and squamate reptiles (lizards and snakes), including documentation in wild populations of both clades. When considered in concert with recent evidence of reproductive competence, the accumulating data suggest that the significance of FP in vertebrate evolution has been largely underestimated. Several fundamental questions regarding developmental mechanisms, nonetheless, remain unanswered. Specifically, what is the type of automixis that underlies the production of progeny and how does this impact the genomic diversity of the resulting parthenogens? Here, we addressed these questions through the application of next-generation sequencing to investigate a suspected case of parthenogenesis in a king cobra (Ophiophagus hannah). Our results provide the first evidence of FP in this species, and provide novel evidence that rejects gametic duplication and supports terminal fusion as a mechanism underlying parthenogenesis in snakes. Moreover, we precisely estimated heterozygosity in parthenogenetic offspring and found appreciable retained genetic diversity that suggests that FP in vertebrates has underappreciated evolutionary significance.
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... All described types could be obligatory or facultative in the different species (Normark 2003). Facultative parthenogenesis, being capable of switching between parthenogenesis and sexual reproduction if the males are absent, is extremely rare among animals (van der Kooi & Schwander 2015). It has been reported in a few insect orders such as mayflies (Ephemeroptera), stick insects (Phasmatodea), grasshoppers and crickets (Orthoptera), and termites and cockroaches (Blattodea) (Went 1982;Sekin e et al. 2015;Riparbelli et al. 2017). ...
Facultative deuterotokous parthenogenesis in Callosobruchus maculatus
Article
  • Jan 2021
  • ZOOL ANZ
The seed beetle, Callosobruchus maculatus (Coleoptera: Chrysomelidae), is a severe cosmopolitan pest of various stored legumes. Since no parthenogenesis has been reported in the genus Callosobruchus, here we report the evidence of a rare event of deuterotokous parthenogenesis in this species. Interestingly, 11.11% of females out of 600 tested virgin females were capable of reproducing by parthenogenesis. Unfertilized-eggs developed into viable adults with a sex ratio of 1:1. Parthenogenetically-produced males and females could successfully copulate and generate the next generation. They achieved statistically the same total immature development, adult longevity, egg number, and hatchability as sexually produced progeny. However, none of the 60 female offspring produced via parthenogenesis were capable of reproducing by parthenogenesis. Mating disruption and sterile insect technique for pest control could not be efficient in insects with parthenogenetic reproduction because parthenogenesis will compensate for males' absence by producing viable male and female offspring, saving species from possible extinction in the future. Therefore, these findings are important not only for considering in the Integrated Pest Management programs but also from an evolutionary perspective. Biodiversity and genetic differentiation among the current worldwide distribution of C. maculatus could be the origin of this facultative deuterotokous parthenogenesis evolution.
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... The presence of specimens with different karyotypes within the same parthenogenetic population supports this hypothesis.Besides polyploidy and hybridization, we can consider the possibility of a mutational origin. Facultative parthenogenesis, where females can reproduce either sexually or asexually, is rare in animals (van derKooi & Schwander, 2015) and has never been reported in Coleoptera (e.g., recent revision papers byNormark, 2014 andGokhman &Kuznetsova, 2018). Nevertheless, although we cannot discard this hypothesis, testing it for N. voeltzkowi requires additional studies, including breeding experiments impossible to perform at this stage due to the absence of collected males. ...
First case of parthenogenesis in ladybirds (Coleoptera: Coccinellidae) suggests new mechanisms for the evolution of asexual reproduction
Article
  • Nov 2019
Parthenogenesis, the development of unfertilized eggs resulting in the exclusive production of female offspring, is rare in animals relative to sexual reproduction and is mainly reported in invertebrates. It has been hypothesized that polyploidy, hybridization and endosymbiont infections are its major causal events but the mechanisms triggering asexual reproduction remain unclear. Here, we study the proximate causes at the origin of parthenogenesis in the first reported case of asexuality in the Coccinellidae (Coleoptera). The asexual populations were found in the Azores and the Mascarene archipelagos, and were identified as Nephus voeltzkowi Weise, a bisexual species widespread in sub‐Saharan Africa. The specimens from both populations are diploid but present different karyotypes and heterozygosities that evoke hybrid origins, commonly associated with parthenogenesis in Coleoptera. However, the close proximity of their genomes (99.8% homology for the complete mitochondrial genome and 99.9% for the complete nuclear ribosomal cluster) together with the congruence between the mtDNA tree and the nuclear tree, and the low heterozygosity levels, suggests that the two populations are not hybrid. We propose that they belong to a single chromosomally polymorphic species undergoing Robertsonian fusions. Furthermore, specimens from both populations are infected with Wolbachia (supergroup B strain), contrary to sympatric bisexual species of the same genus. Although Wolbachia has been shown to induce parthenogenesis in haplodiploid organisms, it has been recently suggested that it could also induce parthenogenesis in hosts with other sex determination systems. Whether chromosome rearrangements and/or Wolbachia infections are post‐parthenogenetic events or are at the origin of parthenogenesis still needs to be determined. We report here the existence of all‐female populations, genetically similar and identified as Nephus voeltzkowi Weise, in the Azores and the Mascarene. Laboratory experiments confirmed they reproduce via thelytokous parthenogenesis, and we combined different approaches to investigate the proximate mechanisms at its origin. Our results reject polyploidization and strongly support a non‐hybrid origin. In contrast, we identified chromosome rearrangements and a Wolbachia infection in parthenogenetic individuals. We cannot exclude they are proximal causes of parthenogenesis.
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Spontaneous parthenogenesis in the parasitoid wasp Cotesia typhae: low frequency anomaly or evolving process?
Article
Full-text available
  • Jun 2022
Hymenopterans are haplodiploids and unlike most other Arthropods they do not possess sexual chromosomes. Sex determination typically happens via the ploidy of individuals: haploids become males and diploids become females. Arrhenotoky is believed to be the ancestral reproduction mode in Hymenopterans, with haploid males produced parthenogenetically, and diploid females produced sexually. However, a number of transitions towards thelytoky (diploid females produced parthenogenetically) have appeared in Hymenopterans, and in most cases populations or species are either totally arrhenotokous or totally thelytokous. Here we present the case of Cotesia typhae (Fernandez-Triana), a Braconidae that produces parthenogenetic females at a low frequency. The phenotyping of two laboratory strains and one natural population showed that this frequency is variable, and that this rare thelytokous phenomenon also happens in the wild. Moreover, mated females from one of the laboratory strains produce a few parthenogenetic daughters among a majority of sexual daughters. The analysis of daughters of heterozygous virgin females allowed us to show that a mechanism similar to automixis with central fusion is very likely at play in C. typhae. This mechanism allows some parts of the genome to remain heterozygous, especially at the chromosomes’ centromeres, which can be advantageous depending on the sex determination system involved. Lastly, in most species, the origin of thelytoky is either bacterial or genetic, and an antibiotic treatment as well as PCR experiments did not demonstrate a bacterial cause in C. typhae. The unusual case of low parthenogenetic frequency described in this species constitutes another example of the fascinating diversity of sex determination systems in Arthropods.
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Mathematical modeling of human oocyte aneuploidy
Article
  • Apr 2020
Aneuploidy is the leading contributor to pregnancy loss, congenital anomalies, and in vitro fertilization (IVF) failure in humans. Although most aneuploid conceptions are thought to originate from meiotic division errors in the female germline, quantitative studies that link the observed phenotypes to underlying error mechanisms are lacking. In this study, we developed a mathematical modeling framework to quantify the contribution of different mechanisms of erroneous chromosome segregation to the production of aneuploid eggs. Our model considers the probabilities of all possible chromosome gain/loss outcomes that arise from meiotic errors, such as nondisjunction (NDJ) in meiosis I and meiosis II, and premature separation of sister chromatids (PSSC) and reverse segregation (RS) in meiosis I. To understand the contributions of different meiotic errors, we fit our model to aneuploidy data from 11,157 blastocyst-stage embryos. Our best-fitting model captures several known features of female meiosis, for instance, the maternal age effect on PSSC. More importantly, our model reveals previously undescribed patterns, including an increased frequency of meiosis II errors among eggs affected by errors in meiosis I. This observation suggests that the occurrence of NDJ in meiosis II is associated with the ploidy status of an egg. We further demonstrate that the model can be used to identify IVF patients who produce an extreme number of aneuploid embryos. The dynamic nature of our mathematical model makes it a powerful tool both for understanding the relative contributions of mechanisms of chromosome missegregation in human female meiosis and for predicting the outcomes of assisted reproduction.
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Different Drosophila cell types exhibit differences in mitotic centrosome assembly dynamics
Article
Full-text available
  • Aug 2015
Centrosomes are major microtubule organising centres comprising a pair of centrioles surrounded by pericentriolar material (PCM). The PCM expands dramatically as cells enter mitosis, and we previously showed that two key PCM components, Centrosomin (Cnn) and Spd-2, cooperate to form a scaffold structure around the centrioles that recruits the mitotic PCM in Drosophila; the SPD-5 and SPD-2 proteins appear to play a similar function in C. elegans[1-3]. In fly syncytial embryos, Cnn and Spd-2 are initially recruited into a central region of the PCM and then flux outwards [4-6]. This centrosomal flux is potentially important, but it has so far not been reported in any other cell type. Here we examine the dynamic behaviour of Cnn and Spd-2 in Drosophila larval brain cells. Spd-2 fluxes outwards from the centrioles in both brains and embryos in a microtubule-independent manner. In contrast, although Cnn is initially incorporated into the region of the PCM occupied by Spd-2 in both brains and embryos, Cnn fluxes outwards along microtubules in embryos, but not in brain cells, where it remains concentrated around the centrosomal Spd-2. Thus, the microtubule-independent centrosomal-flux of Spd-2 occurs in multiple fly cell types, while the microtubule-dependent outward flux of Cnn appears to be restricted to the syncytial embryo. Copyright © 2015 The Authors. Published by Elsevier Ltd.. All rights reserved.
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Isotropic incorporation of SPD-5 underlies centrosome assembly in C. Elegans
Article
Full-text available
  • Aug 2015
Centrosomes are important regulators of microtubule organization in animal cells. Within the centrosome, microtubule nucleation and anchorage are mediated by proteins in the pericentriolar material (PCM) that accumulates around centrioles. The spatial organization of the PCM and the contribution of centrioles to its recruitment remain poorly understood. Previous work in the Drosophila embryo showed that the key PCM component Cnn specifically incorporates near centrioles, suggesting that centrioles play an ongoing role in PCM assembly [1]. It is currently unclear whether this model holds true in other organisms. Here, we examine PCM dynamics in the Caenorhabditis elegans embryo. We find that recruitment of the scaffold component SPD-5 occurs throughout the PCM. Incorporation of additional PCM subunits is therefore not limited to specific nucleation sites near centrioles, which has profound implications for the organization of the PCM lattice and the role of centrioles in centrosome assembly. Copyright © 2015 The Authors. Published by Elsevier Ltd.. All rights reserved.
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Importance of the CEP215-Pericentrin Interaction for Centrosome Maturation during Mitosis
Article
Full-text available
At the onset of mitosis, the centrosome undergoes maturation, which is characterized by a drastic expansion of the pericentriolar material (PCM) and a robust increase in microtubule-organizing activity. CEP215 is one of the major PCM components which accumulates at the centrosome during mitosis. The depletion phenotypes indicate that CEP215 is essential for centrosome maturation and bipolar spindle formation. Here, we performed a series of knockdown-rescue experiments to link the protein-protein interaction properties of CEP215 to its biological functions. The results showed that CEP215 and pericentrin, another major PCM component, is interdependent for their accumulation at the spindle poles during mitosis. As a result, The CEP215-pericentrin interaction is required for centrosome maturation and subsequent bipolar spindle formation during mitosis. On the other hand, CEP215 interaction with γ-tubulin is dispensable for centrosome maturation. Our results provide an insight how PCM components are assembled to form a spindle pole during mitosis.
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Importance of the CEP215-Pericentrin Interaction for Centrosome Maturation during Mitosis
Article
  • Jan 2014
At the onset of mitosis, the centrosome undergoes maturation, which is characterized by a drastic expansion of the pericentriolar material (PCM) and a robust increase in microtubule-organizing activity. CEP215 is one of the major PCM components which accumulates at the centrosome during mitosis. The depletion phenotypes indicate that CEP215 is essential for centrosome maturation and bipolar spindle formation. Here, we performed a series of knockdown-rescue experiments to link the protein-protein interaction properties of CEP215 to its biological functions. The results showed that CEP215 and pericentrin, another major PCM component, is interdependent for their accumulation at the spindle poles during mitosis. As a result, The CEP215-pericentrin interaction is required for centrosome maturation and subsequent bipolar spindle formation during mitosis. On the other hand, CEP215 interaction with c-tubulin is dispensable for centrosome maturation. Our results provide an insight how PCM components are assembled to form a spindle pole during mitosis.
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Binocular Vision: Joining Up the Eyes
Article
  • Aug 2015
To provide a unitary view of the external world, signals from the two eyes must be combined: a new study pinpoints the location in the human brain where the requisite combination occurs. Copyright © 2015 Elsevier Ltd. All rights reserved.
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Facultative parthenogenesis in a critically endangered wild vertebrate
Article
  • Jun 2015
  • CURR BIOL
Facultative parthenogenesis - the ability of sexually reproducing species to sometimes produce offspring asexually - is known from a wide range of ordinarily sexually reproducing vertebrates in captivity, including some birds, reptiles and sharks [1-3]. Despite this, free-living parthenogens have never been observed in any of these taxa in the wild, although two free-living snakes were recently discovered each gestating a single parthenogen - one copperhead (Agkistrodon contortrix) and one cottonmouth (Agkistrodon piscivorus) [1]. Vertebrate parthenogens are characterized as being of the homogametic sex (e.g., females in sharks, males in birds) and by having elevated homozygosity compared to their mother [1-3], which may reduce their viability [4]. Although it is unknown if either of the parthenogenetic snakes would have been carried to term or survived in the wild, facultative parthenogenesis might have adaptive significance [1]. If this is true, it is reasonable to hypothesize that parthenogenesis would be found most often at low population density, when females risk reproductive failure because finding mates is difficult [5]. Here, we document the first examples of viable parthenogens living in a normally sexually reproducing wild vertebrate, the smalltooth sawfish (Pristis pectinata). We also provide a simple approach to screen any microsatellite DNA database for parthenogens, which will enable hypothesis-driven research on the significance of vertebrate parthenogenesis in the wild. Copyright © 2015 Elsevier Ltd. All rights reserved.
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On the Evolution of Parthenogenesis in Lonchoptera (Diptera)
Article
  • Dec 1956
1. A study of chromosomal variability in the diploid parthenogenetic species Lonchoptera dubia Curran (Lonchopteridae, Brachycera, Diptera) is described. This study is based on an analysis of 272 females from 32 widely separated areas, chiefly in eastern North America. 2. L. dubia is almost entirely nearctic and northern in distribution, occurring in the northern United States and southern Canada. It is collected by sweeping, principally from the White Clover-Plantain complex characteristic of pastures, lawns, etc. 3. In this species the nuclei of the mature ovarian nurse cells contain large, banded polytene chromosomes similar to those of Drosophila salivary glands. There are four polytene chromosome arms, and the banding patterns of three of these were studied in detail. On the basis of the eleven known sequences for these three arms the species may be divided into four chromosomal races which show distinctly different, but overlapping, geographical ranges. In many localities two or more chromosomal races were taken with a single sweep of the collecting net. 4. The four chromosomal races are permanent structural heterozygotes for some or all chromosome arms. Study of Feulgen whole-mounts of freshly-laid eggs indicated that L. dubia is automictic (meiotic), with two meiotic divisions followed by a fusion of two of the four haploid meiotic products. The absence of adult structural homozygotes in wild populations is probably explained by death during early development (occurring in at least 25% of eggs) and by possible fusion of second-division meiotic products derived from different secondary oocytes, which if occasional crossovers are disregarded, would exactly reconstitute the original heterozygosity of the mother. 5. In the eastern part of the range small but significant differences in the wing-vein dimensions occur between the populations made up of Races 1 and 2 and those made up of Races 3 and 4. 6. The micro-distributions of the various chromosomal races make it clear that they are not wholly competitive. If they were, one race would replace others in a given micro-habitat. Thus the four races are chromosomally, ecologically, and genetically different. 7. Selection studies on the automictic (normally bisexual) tychoparthenogenetic species DrosophiIa parthenogenetica indicate that continued selection for parthenogenesis within a unisexual line for 62 generations results in selective improvement in parthenogenesis during the first 17 generations, and thereafter no change in rate of parthenogenesis. However, crossing between the unisexual line and an ancestral bisexual one brings about marked selective advance in rate of parthenogenesis. 8. It is suggested that in L. dubia parthenogenesis has arisen gradually within extensive semi-isolated small populations of the bisexual ancestor. In such small populations sampling error would bring about recurrent male-shortages, resulting in selective advantage to parthenogenetic development. In time, as genotypes permitting parthenogenesis were built up in the small populations, the male-shortages would become increasingly acute and selection would be intensified. Crossing between different populations would allow more effective synthesis of parthenogenetic genotypes, at the same time 'freezing' into the developing unisexual races much of the chromosomal variability originally present in the bisexual ancestor. Finally when all males were lost, further selective improvement in parthenogenesis might be slowed down or stopped, leaving the species with an imperfect parthenogenetic mechanism. Additional support for this hypothesis comes from the fact that the bisexual species, L. occidentalis, does have complex structural variability of the sort postulated for the bisexual ancestor of L. dubia, and also from the fact that parthenogenesis in L. dubia is imperfect, with about 9% of the eggs failing to show any development.
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