PARTHENOGENESIS
Parthenogenesis without costs in a grasshopper with
hybrid origins
Michael R. Kearney^1 *, Moshe E. Jasper^2 , Vanessa L. White^1 , Ian J. Aitkenhead^3 , Mark J. Blacket^1 †,
Jacinta D. Kong^1 ‡, Steven L. Chown^3 , Ary A. Hoffmann^2
The rarity of parthenogenetic species is typically attributed to the reduced genetic variability that
accompanies the absence of sex, yet natural parthenogens can be surprisingly successful. Ecological
success is often proposed to derive from hybridization through enhanced genetic diversity from
repetitive origins or enhanced phenotypic breadth from heterosis. Here, we tested and rejected both
hypotheses in a classic parthenogen, the diploid grasshopperWarramaba virgo. Genetic data revealed a
single hybrid mating origin at least 0.25 million years ago, and comparative analyses of 14 physiological
and life history traits showed no evidence for altered fitness relative to its sexual progenitors.
Our findings imply that the rarity of parthenogenesis is due to constraints on origin rather than to
rapid extinction.
T
he dominance of sexual reproduction
over parthenogenesis remains a mys-
tery in evolutionary biology ( 1 , 2 ). By
dispensing with males, parthenogenetic
lineages instantly double their population
growth rate ( 3 ) and should thus be strongly
selected ( 1 ). Parthenogenetic lineages can
be highly successful ( 4 ) but are exceedingly
rare: 99.9% of species reproduce sexually ( 1 ).
In the long run, parthenogenetic lineages are
expected to become extinct because, in the
absence of sexual genetic recombination, they
areunabletoadaptthroughnewcombina-
tions of adaptive alleles and are more suscep-
tible to accumulating deleterious mutations
( 5 ). However, when parthenogenetic species
do arise, they often spread rapidly and beyond
the ranges of their sexual progenitors ( 4 , 6 ).
This pattern, called“geographic partheno-
genesis”( 4 ), could reflect demographic con-
sequences of parthenogenesis per se, which
include a twofold reproductive advantage,
not having to find a mate, and“heterozygosity
assurance”( 7 ) arising from clonal reproduc-
tion. Given these advantages and the well-
documented examples of highly successful
parthenogens, the rarity of parthenogenesis
remains puzzling.
A challenge in assessing reasons for the
success of parthenogenesis is that it frequently
arises in association with hybridization and
polyploidy ( 6 ). Parthenogenesis may not be
selected directly for its demographic conse-
quences, but rather may fix advantageous
hybrid or polypoid“general purpose geno-
types”( 4 , 8 ) or freeze ecologically distinct
genotypes captured by repetitive hybridization
events (the“frozen niche variation hypothe-
sis ”)( 6 , 9 ). Alternatively, hybridization may act
to trigger asexual reproduction if incompat-
ibilities between parental genomes disrupt
meiosis without greatly reducing overall fit-
ness (the“balance hypothesis”)( 10 , 11 ).
Studying natural cases of parthenogenesis
in detail helps to resolve these issues. Here, we
focused on the classic case of parthenogenesis
involving the Australianwingless grasshopper
Warramaba virgo( 12 ), analyzing extensive
data on its genetics, ecophysiology, life history,
and distribution compared with its sexual
progenitors.W. virgois diploid and sperm
independent, and thus does not suffer from
the interpretive complications associated with
polyploidy or the potential for rare sex. It also
has morphological diversity similar to its sex-
ual progenitors and feeds on a wide range of
plants ( 13 ). Previous evidence demonstrated
that this species evolved by hybridization
between the sexual speciesWarramaba whitei
andWarramaba flavolineata, unveiling 21
clones among 100 individuals, suggesting
that much of this diversity could be explained
by repetitive hybrid origins ( 14 , 15 ). Hybrid-
ization between these taxa also produced
the morphologically separate parthenogen
Warramaba ngadju( 12 ). Both parthenoge-
netic species occur to the south of their pro-
genitors in Western Australia, andW. virgo
has expanded >2000 km to the east, with a
1600-km gap across an arid region (the Nullarbor
Plain; Fig. 1). Thus, the ecological success of
W. virgoacross a broad geographic range
could stem primarily from its hybrid state if
repetitive origins produced ecologically diverse
clones (frozen niche variation) or if heterosis
enhanced its fitness or ecological breadth
(general purpose genotype).
To test these hypotheses, we genotyped 142
W. virgo,43W. whitei,and41W. flavolineatafor 1539 polymorphic single-nucleotide poly-
morphism (SNP) loci,sampling across the
known range of all taxa (fig. S1 and table S1).
Our SNP data demonstrated thatW. virgo
arose as a single clone that spread rapidly
across the landscape, and that the genetic
variation observed in this species is post-
formational. Genetic distances between indi-
vidual parthenogens within and between
populations were two orders of magnitude
lower than equivalent distances for sexual taxa
(Fig. 2 and figs. S2 and S3). Parthenogenetic
individuals from the same population were
more similar to each other than to other
populations (figs. S4 and S5), but there was
little distinction between populations span-
ning the east-west gap. Therefore, isolation
by distance (IBD) in the parthenogens was
absent compared with a moderate IBD sig-
nal in the sexual species when estimated from
the number of common alleles (figs. S6 and S7).
Thepresenceofsomepopulationdifferentia-
tion inW. virgodespite a lack of IBD suggests
local clonal selection after colonization of an
area and/or bottlenecks but is inconsistent
with a gradual range expansion byW. virgo.
Our data also clearly reject the possibility of
any introgression of genes toW. virgofrom
the parapatric sexual populations in Western
Australia.
The SNP variation across all individuals
(Fig. 3 and fig. S8) reveals much more vari-
ation in the sexual species compared with
the parthenogens, which was supported by
a more geographically extensive analysis of
five microsatellite markers inW. virgo(figs.
S9 and S10 and tables S2 and S3). Although
a prior allozyme study interpreted the varia-
tion as reflecting repetitive origins ofW. virgo
hybrids ( 15 ), our new nuclear DNA data do
not support repetitive origins, and thus al-
lozyme variation must be reinterpreted as
postformational. Moreover, our findings of
geographic clustering in SNP variation is con-
sistent with the geographical localization of
the many cytological clones found in early
studies ofW. virgo( 16 ). The second parthe-
nogen,W. ngadju, has similarly low genetic
variation ( 14 , 17 ).
Patterns of heterozygosity inW. virgofit a
hybrid origin but with biases probably result-
ing from gene conversion events since the
species’origin [compare ( 18 )]. Many individ-
uals were heterozygous for the same SNPs
(Fig. 3, white areas). Of the 1164 biallelic SNP
loci common to all three taxa, 53% were largely
fixed for different alleles in the sexual species
and heterozygous for these alleles in the
parthenogens, as would be expected under
a diploid hybrid origin. Another 23% were
fixed for the same allele in the sexual species
but were heterozygous in the parthenogens,
20% were homozygous in the parthenogens
and fixed for this allele in one but not theRESEARCH
Kearneyet al., Science 376 , 1110–1114 (2022) 3 June 2022 1of4
(^1) School of BioSciences, The University of Melbourne, Victoria
3010, Australia.^2 Bio21 Institute, School of BioSciences, The
University of Melbourne, Victoria 3010, Australia.^3 School of
Biological Sciences, Monash University, Victoria 3800,
Australia.
*Corresponding author. Email: [email protected]
†Present address: Agriculture Victoria, AgriBio Centre, Bundoora,
Victoria 3083, Australia.‡Present address: School of Natural
Sciences, Trinity College Dublin, Dublin 2, Ireland.