Meiotic drive does not cause condition‐dependent reduction of the sexual ornament in stalk‐eyed flies

Abstract

Meiotic drive systems are associated with low frequency chromosomal inversions. These are expected to accumulate deleterious mutations due to reduced recombination and low effective population size. We test this prediction using the "sex-ratio" (SR) meiotic drive system of the Malaysian stalk-eyed fly Teleopsis dalmanni. SR is associated with a large inversion (or inversions) on the X chromosome. In particular, we study eyespan in males carrying the SR chromosome, as this trait is a highly exaggerated, sexually dimorphic trait, known to have heightened condition-dependent expression. Larvae were raised in low and high larval food stress environments. SR males showed reduced eyespan under the low and high stress treatments but there was no evidence of a condition-dependent decrease in eyespan under high stress. Similar but more complex patterns were observed for female eyespan, with evidence of additivity under low stress and heterosis under high stress. These results do not support the hypothesis that reduced sexual ornament size in meiotic drive males is due to a condition-dependent response to the putative increase in mutation load. Instead, reduced eyespan likely reflects compensatory resource allocation to different traits in response to drive-mediated destruction of sperm.

Full text

J Evol Biol. 2021;00:1–10.
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1wileyonlinelibrary.com/journal/jeb
1 | INTRODUCTION
A key tenet of the handicap principle (Grafen, 1990; Iwasa
et al., 1991; Zahavi, 1977) is that sexual ornaments show height-
ened condition- dependent expression (Cotton et al., 20 04a;
Pomiankowski & Møller, 1995; Rowe & Houle, 1996). Historically,
empirical support was limited as studies omitted comparisons
with nonsexual control trait s (Cotton et al., 2004a). But there
are a growing number of studies showing that heightened con-
dition dependence is a feature of many sexual traits used in mate
preference (Bonduriansky & Rowe, 2005; Izzo & Tibbet ts, 2015;
Johns et al., 2014). A canonical example is eyespan in the Malaysian
stalk- eyed fly, Teleopsis dalmanni (Cotton et al., 2004b). Stalk- eyed
flies are characterized by lateral elongation of the head capsule into
eyestalks (Wilkinson & Dodson, 1997). Many species of stalk- eyed
fly, including T. dalmanni, are highly sexually dimorphic for this trait,
with males possessing much larger eyespan than females (Baker
& Wilkinson, 2001). Eyespan is used as a signal in female choice
(Hingle et al., 2001; Wilkinson & Reillo, 1994) and male– male inter-
actions (Panhuis & Wilkinson, 1999; Small et al., 2009). In the wild,
Received: 25 Septem ber 2020
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Revised: 25 Ja nuary 2021
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Accepted: 27 January 2 021
DOI : 10.1111 /je b.137 70
RESEARCH PAPER
Meiotic drive does not cause condition- dependent reduction of
the sexual ornament in stalk- eyed flies
Sam Ronan Finnegan1 | Matteo Mondani1 | Kevin Fowler1 |
Andrew Pomiankowski1,2
This is an op en access article under t he terms of the Creat ive Commons Attributio n License, which permits use, dist ribution and reproduc tion in any medium,
provide d the orig inal work is proper ly cited .
© 2021 The Authors. Journal of Evolutiona ry Biol ogy published by John Wiley & S ons Ltd on behalf of European So ciety for Evolutio nary Biology.
1Department of Genetics, Evolution and
Environment, University College London,
London, UK
2CoMPLE X, Universit y College London,
London, UK
Correspondence
Andrew Pomiankowski, Department of
Genetics, Evolution and Environment,
University College London, Gowe r Street ,
London WC1E 6BT, UK.
Email: ucbhpom@ucl.ac.uk
Funding information
Engineering and Physical Sciences Research
Council, Grant/Award Number: EP/
F500351/1 and EP/I017909/1; Natural
Environment Research Council, Grant/
Award Number: NE/L002485/1, NE/
G00563X/1 and NE/R010579/1
Abstract
Meiotic drive systems are associated with low- frequency chromosomal inversions.
These are expected to accumulate deleterious mutations due to reduced recombina-
tion and low effective population size. We test this prediction using the ‘sex- ratio’
(SR) meiotic drive system of the Malaysian stalk- eyed fly Teleopsis dalmanni. SR is
associated with a large inversion (or inversions) on the X chromosome. In particular,
we study eyespan in males carrying the SR chromosome, as this trait is a highly exag-
gerated, sexually dimorphic trait, known to have heightened condition- dependent
expression. Larvae were raised in low and high lar val food stress environments. SR
males showed reduced eyespan under the low and high stress treatments, but there
was no evidence of a condition- dependent decrease in eyespan under high stress.
Similar but more complex patterns were observed for female eyespan, with evidence
of additivity under low stress and heterosis under high stress. These results do not
support the hypothesis that reduced sexual ornament size in meiotic drive males is
due to a condition- dependent response to the putative increase in mutation load.
Instead, reduced eyespan likely reflects compensatory resource allocation to differ-
ent traits in response to drive- mediated destruction of sperm.
KEYWORDS
condition dependence, meiotic drive, sexual ornament, sexual selection, stalk- eyed fly

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females prefer to roost and mate with males with larger eyespan,
both in absolute terms and relative to body size (Cotton et al., 2010;
Wilkinson & Reillo, 1994). Male eyespan is highly sensitive to both a
range of environmental (Bjorksten et al., 2001; Cotton et al., 20 04a;
David et al., 1998) and genetic stresses (Bellamy et al., 2013; David
et al., 2000; Howie et al., 2019).
The sexual ornament in T. dalmanni is also associated with se x-
ratio meiotic drive (SR), a common type of selfish genetic element
located on the X chromosome that causes selective destruction of
Y- bearing sperm and the production of female- biased broods (Hurst
& Pomiankowski, 1991; Jaenike, 2001; Lindholm et al., 2016). The
XSR chromosome exists at moderate frequencies (~20%) in wild
populations (Cotton et al., 2014; Paczolt et al., 2017; Wilkinson
et al., 2003). Male carriers of XSR have reduced eyespan both
under laborator y conditions (Johns et al., 2005; Meade et al., 2019;
Wilkinson et al., 1998) and in the wild (Cotton et al., 2014). The drive
and standard (XST) chromosomes are differentiated by a large para-
centric inversion (or inversions; Johns et al., 20 05), spanning at least
one third of the chromosome (Paczolt et al., 2017). Inversions are a
common feature of many meiotic drive systems that restrict recom-
bination (Hoffmann & Rieseberg, 2008; Kirkpatrick, 2010) and are
presumed to have been selected to maintain linkage on XSR between
genes contributing to meiotic drive (Charlesworth & Hartl, 1978;
Jaenike, 2001). The lack of recombination between XSR and XST has
contributed to their divergence, with multiple differences becoming
fixed (Reinhardt et al., 2014) over an estimated half million year sep-
aration (Paczolt et al., 2017; Swallow et al., 2005).
Long- term recombination suppression within drive- associated
inversions is expected to lead to a weaker response to selection and
an increase in the accumulation of deleterious mutations (Gordo &
Charlesworth, 2001), as ob served in extremis on Y chromosomes (Orr
& Kim, 1998). Several meiotic drive inversions are associated with
mutations that severely impac t fitness (Jaenike, 2001). For example,
in the t- haplotype autosomal drive system in the house mouse, Mus
musculus, many drive haplotypes carry factors that cause embr yonic
lethalit y when homozygous (Silver, 1985). In Drosophila recens, the
entire SR drive X chromosome is composed of a series of overlapping
inversions and is fixed for a recessive mutation causing female ste-
rility (Dyer et al., 2007). In the stalk- eyed fly, there are a large num-
ber of fixed sequence differences between XSR and XST (Reinhardt
et al., 2014) and carriers of the XSR chromosome have reduced egg-
to- adult viability in both sexes (Finnegan et al., 2019). These findings
suggest that the XSR haplotype carries an increased mutation load,
leading to an overall reduction in genetic quality. We hypothesized
that this should be reflected in a condition- dependent reduction of
eyespan, with the dif ference between SR and ST male eyespan being
small under low environmental stress and large when environmental
stress is high, since the reduced genetic quality of SR males should
render them less able to cope with stressful conditions.
There is some evidence that the X chromosome in T. dalmanni
is associated with additive genetic variance for eyespan. In a quan-
titative trait locus (QTL) study, Johns et al., (2005) found a major
X- linked QTL associated with small male eyespan, located just 1.3cM
from the putative drive locus. In addition, Reinhardt et al., (2014)
used RNAseq to identify transcripts that are differentially expressed
between XSR and XST males. Although many of these transcripts
were associated with testis development, as might be expected,
a group of transcript s were associated with eye development, in-
cluding two genes— chiffon and CG 4598— that had previously been
shown to be differentially expressed in stalk- eyed flies artificially
selected for long and short eyespan (Baker et al., 20 09). However,
neither of these studies considered whether these putative markers
had condition- dependent effects on male eyespan.
Understanding the evolution and maintenance of male sex-
ual ornaments has been the central focus of a wide body of
work. Homologous female traits have received less at tention
(Amundsen, 2000). The evolution of the female trait is thought to
reflect selection on males for exaggeration coupled to a shared ge-
netic architecture opposed by counter- veiling selection on female
eyespan (Lande, 1980; Tobias et al., 2012). More recently, it has been
recognized that female traits may also act as signals of mate quality
maintained by male mate preferences (Amundsen, 20 00) or female–
female com petition (LeBas, 2006). In stalk- eyed flies, fem ale eyespan
is an indicator of fecundity, and so males prefer to mate with females
with large eyespan (Cotton et al., 2010, 2015; Finnegan et al., 2020).
Large eyespan females also manifest stronger mate preference for
large males as they are better able to distinguish variation in male
eyespan (Hingle et al., 2001). In addition, female eyespan shows
heightened condition- dependent expression, although to a lesser
extent than male eyespan (Cotton et al., 2004b). To date, there is
mixed evidence that the XSR affects female eyespan. The X- linked
QTL linked to meiotic drive explains over a third of the variation in
male eyespan but just 9% of the variation in female eyespan (Johns
et al., 2005). In wild flies, no association was found between female
eyespan and ms395 allele size, a marker that is strongly associated
with meiotic drive and male relative eyespan (Cotton et al., 2014).
As female eyespan acts as a trait involved in sexual selection with
heightened condition dependence, the relationship between the
putative lower genetic quality of the XSR haplotype and female
eyespan warrants further study. We predicted that the putative in-
creased mutation load on the XSR should be reflected in condition-
dependent expression of female eyespan, although to a lesser extent
than in males.
Here, we used manipulations of larval dietary stress to deter-
mine how environmental stress interacts with the XSR haplot ype to
affect condition- dependent expression of male and female eyespan.
We reared lar vae of all possible male and female XSR and XST gen-
otypes under two food treatments— low and high food stress— and
examined the resulting variation in eyespan. Our aims were to deter-
mine whether SR and ST male eyespan differs when flies are reared
under low stress, and whether high environmental stress amplifies
this difference, as expected if the XSR chromosome is associated
with reduced genetic quality. We predicted that XSR would have a
similar, but weaker, condition- dependent effect on the expression
of female eyespan. We also estimated the dominance relationship
for eyespan, by comparing homozygous standard, heterozygous and

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FINNEGAN E t Al.
homozygous drive females. Since mildly deleterious effects are gen-
erally recessive (Charlesworth & Willis, 2009; Fry & Nuzhdin, 2003),
our expectation was that homozygous drive females would show a
disproportionate reduction in eyespan.
2 | MATERIALS AND METHODS
2.1 | Stocks
A standard (ST) stock was obtained from Ulu Gombak in Malaysia
(3°190N 101°450E) in 2005 by Andrew Pomiankowski and Sam
Cotton. Meiotic drive (SR) is absent from the standard stock. Flies
are maintained in high- density cage culture (cage size approx.
30 × 20 × 20 cm) at 25°C with a 12- hr light:dark cycle that includes
15- min ar tificial dawn- and- dusk periods. Stock flies are fed 100%
corn ad libitum.
A meiotic drive stock was obtained in 2012 by Sam Cotton from
the same Ulu Gombak location. Meiotic drive is maintained follow-
ing a standard protocol (Meade et al., 2020; Presgraves et al., 1997).
Briefly, females heterozygous for SR (XSRXST ) are crossed to ST
(XSTY) males and the female offspring are discarded. The male off-
spring from this cross, half of which are expected to have inherited
SR, are crossed individually to ST (XSTXST) females, and their off-
spring sex ratio is recorded. Males that produce all- female broods of
15 or more are considered SR (XSRY). Drive strength is 100% in the
SR stock so SR males do not sire any male of fspring. All offspring of
SR males are heterozygous females that are then mated to ST males,
and the process is repeated. We note that our breeding protocol has
resulted in fixation in the stock of a single XSR haplotype, causing
strong drive. The distribution of brood sex ratios among wild- c aught
flies is considerably more variable (Cotton et al., 2014; Wilkinson
et al., 2003), which is also the case under other laboratory breeding
regimes (Meade et al., 2019; Wilkinson et al., 1998). This variation
remains to be investigated.
2.2 | Experimental flies
Experimental females used in crosses were heterozygous for SR, taken
from the SR stock. To obtain experimental males with known geno-
types, males were collected from the SR stock and crossed individually
to ST females. Their larvae were genotyped for SR to determine the
paternal genotype (for genotyping details, see below). Larvae from SR
males were heterozygous for SR, whereas larvae from ST males were
either females homozygous for ST or males hemizygous for ST.
2.3 | Experimental crosses and egg collection
In order to produce all f ive genotypes ( XSTXST, XSRXST, XSRXSR females
and XSTY, XSRY males), two crosses were employed following a stand-
ard design (Finnegan et al., 2019). In Cross A , XSRXST females were
crossed to XSRY drive males (5 of each per cage), generating XSRXST
and XSRXSR females. In Cross B, XSR XST females were crossed to XST Y
males (5 of each per cage), generating XSTXST and XSRXST females,
and XSTY and XSRY males. Four replicates were set up for Cross A
and eight for Cross B. Eg gs wer e collec te d daily (i.e. when ≤24 hr ol d),
and groups of 12 were alloc ated per Petri dish; each dish contained
a damp cotton wool pad and food. Two larval food treatments were
used, based on earlier work (Cotton et al., 2004b). High stress was
allocated 0.03 g of pureed sweetcorn per egg, and low stress was
allocated 0.12 g per egg. Adults were collected as they eclosed and
frozen for later measurement of eyespan (the distance between the
distal tips of the eye bulbs) and thorax length (the distance bet ween
the anterior- most point of the prothorax and the posterior- most edge
of the thorax; Cotton et al., 20 04b), using ImageJ (v.1.46). Measured
flies were then stored in 100% ethanol for genotyping.
A second experiment was carried out using identical food treat-
ments and rearing conditions. However, eggs from Cross A and
Cross B were no longer reared separately but instead mixed to-
gether in each Petri dish. Four eggs from Cross A were mixed with
eight eggs from Cross B, generating all genotypes (XSTXST, XSRXST,
XSRXSR females and XSTY, XSRY males) in a 1:2:1:1:1 ratio on average.
This design was used previously for measuring egg- to- adult survival
(Finnegan et al., 2019). Morphology measures of eclosed adults were
obtained in the same way as in the first experiment .
2.4 | Genotyping
To extract DNA, the abdomen of each fly was removed and placed in
a 96- well plate containing 50 μl of squish buffer (5 μl 10× Taq Buffer
with KCL and 15 mM MgCl2 (Thermo Scientific), 3 μl proteinase K and
42 μl UltraPure H2O). Abdomens were mechanically lysed, and wells
were topped up with a further 100 μl squish buffer. The 96- well plates
were then transferred to a 2,720 Thermal Cycler (Applied Biosystems)
and incubated at 37°C for 30 min, before being heated to 95°C for
3 min to denature the proteinase K. Extracted DNA was stored at 4°C.
DNA was PCR- amplified on a 2720 Thermal Cycler (Applied
Biosystems) in 96- well plates containing 1 µl of DNA, 0.1 µl of 5×
Phusion Taq polymerase (New England BioLabs), 0.2 µl of dNTPs,
6.2 µl UltraPure water and 0.5 µl each of the 10 µM forward and
reverse primers for comp162710. Comp162710 is an indel marker
developed in the laboratory of Jerry Wilkinson (personal com-
munication) to identify XSR chromosomes that carr y a small allele
(201 bp) and XST chromosomes that carry a large allele (286 bp). This
marker has been successfully used previously (Meade et al., 2020).
Comp167210 fragment lengths were assayed by gel electrophoresis
on a 3% agarose gel with a 0.5× TBE buffer.
2.5 | Statistical analysis
The effects on absolute male eyespan of food treatment, genotype,
and the food treatment by genotype interaction were analysed in a

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FINNEGAN Et Al.
linear model. Then, the effect on residual eyespan was analysed by
including thorax in the model. Female eyespan was analysed using
similar models and including a factor for parental cross. As paren-
tal cross had a strong effect on female eyespan, the data were split
by cross and reanalysed. In a further analysis, we controlled for the
effect of cross by adjusting Cross B female eyespan values by the
percentage difference between heterozygous XSRXST eyespan in
Cross A and Cross B. Pairwise comparisons of female genotypes
were made using Tukey's post hoc comparison tests. We report all
model effects in the Supplementary information. The effect of food
treatment, genot ype and their interaction on thorax length is also
included in the Supplementary information.
3 | RESULTS
3.1 | Male eyespan
A total of 468 males were collected, of which 423 were successfully
genotyped. Food treatment had a strong effect on absolute male eye-
span, which was smaller under the high stress food treatment (mean ±
SE, low stress = 7.86 9 3 ± 0.0660 mm, high stress = 4.6893 ± 0.0609,
F1,416 = 1,188.1578, p < .0001; Figure 1). SR males had smaller eye-
span than ST males overall (F1,416 = 5.1820, p = .0233), although this
was only evident under low stress (mean ± SE, SR = 7.78 53 ± 0.0958,
ST = 7.9638 ± 0.0981, F1,216 = 9.3255 p = .0025) and not under high
stress (mean ± SE, SR = 4. 5749 ± 0.0907, ST = 4.7824 ± 0.0934,
F1,199 = 2.5466, p = .1109; Figure 1). The magnitude of the difference
between SR and ST males did not differ between low and high stress
(food treatment by genot ype interaction, F1,416 = 0.12 29, p = .7261) .
After controlling for body size, residual male eyespan was still st rongly
affected by food treatment (F1, 413 = 90.0744, p < .0001). SR males had
reduced residual eyespan compared with ST males (F1,413 = 8. 5065,
p = .0037), and again, the magnitude of this difference did not change
across food treatment (F1,413 = 0.2786, p = .5979).
3.2 | Female eyespan
A total of 1,159 females were collected, of which 1,086 were suc-
cessfully genotyped. As in males, the high stress food treatment
had a strong negative effect on absolute female eyespan (mean ±
SE, low stress = 5.6557 ± 0.0188, high stress = 4.1473 ± 0.0209,
F1,1,063 = 2,824.0524, p < .00 01). There was a significant effect of
cross on female eyespan (F1,1,063 = 5.7000, p = .0171), so genotypes
were compared separately for Cross A and Cross B (Figure 2). XSR
homozygotes had smaller absolute eyespan than heteroz ygous
females (F1,586 = 6 .14 3 7, p = .0135). There was a significant food
treatment by genotype interaction (F1,586 = 4.0962, p = .043 4) as
XSR homozygotes were smaller than heterozygotes under high stress
(mean ± SE, XSRXST = 4. 2421 ± 0.0409, XSRXSR = 4.0958 ± 0.0399,
F1,331 = 7.9 4 8 3 , p = .0051) but not under low stress (mean ± SE,
XSRXST = 5.7118 ± 0.0401, XSRXSR = 5.7096 ± 0.03 47, F1,254 = 0.0274,
p = .8687). In Cross B, absolute female eyespan did not differ be-
tween heterozygotes and XST homozygotes under high (mean ± SE,
XSTXST = 4.0866 ± 0.0415, XSRXST = 4.1947 ± 0.0489, F1,266 = 2.9528,
p = .0883) or low stress (mean ± SE, XSTXST = 5.6153 ± 0.0415,
XSRXST = 5.5876 ± 0.0398, F1,208 = 1.193 3, p = .2759), nor was there
a food treatment by genotype interaction (F1,475 = 2.8 579, p = .0916).
After controlling for body size, genotype no longer explained
variation in residual female eyespan in Cross A (F1,585 = 0.0703,
p = .7910) or Cross B (F1, 474 = 0.1824, p = .6695), and there was
no food treatment by genotype interaction in either cross (Cross A,
F1,585 = 0.2084, p = .6482; Cross B, F1 ,474 = 0.2221, p = .6377).
FIGURE 1 Absolute male XSRY (red) and XSTY (blue) eyespan
in low and high stress larval food treatments. Boxes enclose 1st
and 3rd quartiles, with whiskers extending to 1.5×IQR. Thick black
lines within boxplots show the medians. Significance values reflect
p- values obtained from models where males were split into low and
high stress, as opposed to those given by the full model presented
in Results section. ** p < .01
FIGURE 2 Absolute female eyespan in low stress and high
stress larval food treatments, where females from each cross
category were reared separately. Cross A produces XSR XSR (orange)
and XSRXST (green) genotypes. Cross B produces XSTXSR (green)
and XSTXST (purple) genotypes. For details of the presentation, see
Figure 1. * p < .05

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FINNEGAN E t Al.
To compare the three female genotypes (Figure 3), we controlled
for cross by equalizing measurements of female heterozygotes,
which were common to Cross A and Cross B (see Methods). Absolute
eyespan depended on genotype (F2,1,064 = 4 . 699 7, p = .0093), and
the effect of genot ype varied across food treatment (food treatment
by genotype interaction, F2 ,1,06 4 = 3. 4041 , p = .0336). Under low
stress, XST homozygous females had the largest absolute eyespan
(mean ± SE = 5.74 013 ± 0.0425), which was larger than XSR homozy-
gous females (mean ± SE = 5.7096 ± 0.0347; Tukey's test, p = .0026).
Heterozygous females had intermediate absolute eyespan (mean ±
SE = 5.7118 ± 0.0285), n ot different fro m either homozygo te (Tukey's
XSTXST – XSTXSR comparison, p = .0508; X SRXST – XSRXSR comparison,
p = .3581). Under high stress, heterozygous females had the largest
absolute eyespan (mean ± SE = 4.2422 ± 0.0315), larger than XSR ho-
mozygotes (mean ± SE = 4.0958 ± 0.0399, Tukey's test, p = .0040)
but not larger than XST homozygotes (mean ± SE = 4.1328 ± 0.0420,
Tukey's test, p = .1303). As before, when controlling for body size
genotype did not affect residual female eyespan (F2,1,063 = 0. 5 412 ,
p = .5822), and there was no food treatment by genotype interaction
(F2,1,063 = 0.5656, p = .5682).
3.3 | Female eyespan (second experiment)
In a second experiment, eggs from Cross A and Cross B were mixed
together, so that all genotypes potentially emerged from the same
Petri dish. In particular, this eliminated specific differences associ-
ated with Cross A and Cross B among the three female genotypes,
and avoids the need to equalize them statistically. Female absolute
eyespan again depended on food treatment (F1,446 = 1,678.7142,
p < .0001) and genotype (F2,446 = 5.6035, p = .0039). There was no
food treatment by genotype interaction (F2,446 = 2.0007, p = .136 4).
However, the largest genotype was dif ferent across the treatment s.
In low stress, XSTXST eyespan (mean ± SE = 6. 0766 ± 0.0252) is larger
than XSR XSR (mean ± SE = 5.9246 ± 0.0352; Tukey's test, p = .0 02)
and XSRXST is intermediate (mean ± SE = 5.9888 ± 0.02659; Tukey's
XSRXST – XSTXST comparison, p = .0872, XSRXST – XSR XSR com-
parison, p = .2529). In high stress, heterozygous XSRXST eyespan
(mean ± SE = 4.4860 ± 0.0577) is larger than XSR XSR (mean ±
SE = 4.2596 ± 0.0691; Tukey's test, p = .0424) and XST XST is inter-
mediate (mean ± SE = 4.4257 ± 0.0676, Tukey's XSRXST – XSTXST
comparison, p = .7784, XSRXST – XSRXSR comparison, p = .2498).
After controlling for body size, genotype affected residual eye-
span in low stress (F2, 246 = 4 .7519, p = .0094), but not in high stress
(F2,198 = 1 .5412, p = .2167). The results from the second experi-
ment are therefore in broad agreement with those from the first
experiment.
4 | DISCUSSION
Male eyespan in stalk- eyed flies is a canonical example of an exag ger-
ated sexua l character that i s highly condition- dep endent, in respo nse
to both environmental (Cotton et al., 200 4b; David et al., 1998)
and genetic stress (Bellamy et al., 2013; David et al., 2000; Howie
et al., 2019). T. dalmanni stalk- eyed flies show reduced eyespan in
males carrying SR meiotic drive. Here, we tested the hypothesis that
this reduction is a condition- dependent response arising from the
low genetic quality of the XSR chromosome. As reported previously
(Cotton et al., 2010; Wilkinson et al., 1998), eyespan was reduced
in SR males and this effect persisted af ter controlling for body size
(Figure 1). But the difference in eyespan between males carr ying the
XSR and XST chromosomes was not condition- dependent; there was
no evidence for amplified reduction in the sexual ornament of SR
males under high environmental stress.
The environmental stress used in this study follows previ-
ous work on stalk- eyed flies using larval food reduc tions (Cot ton
et al., 2004b), which has a similar effect to other stresses, such as
thermal shock and desiccation (Bjorksten et al., 2001). The ‘low’
stress treatment constituted a plentiful amount of the standard lab-
oratory food. The ‘high’ stress treatment was chosen using previous
work, at a level at which eyespan subst antially declined but before
any large increase in mortality (Cotton et al., 20 04b). Previous
work has also shown that genetic differences in the male sexual
ornament are constrained under low stress but amplified as envi-
ronmental stress increases (Bellamy et al., 2013; David et al., 200 0;
Howie et al., 2019). This is not the pat tern observed here as the
smaller eyespan of SR males was consistent across environmental
stress treatments (Figure 1). This pattern is further supported by
prior experiment al work using dietar y stress based on varying pro-
tein: carbohydrate ratios (rather than var ying the amount of food
per larva), where SR male eyespan was reduced relative to ST, but
no amplification was repor ted as the protein content of the diet
declined (Cotton, 2016).
The lack of an amplified reduction in SR male eyespan under en-
vironmental stress is not consistent with the expected low genetic
FIGURE 3 Absolute eyespan of XSRXSR (orange), XSRXST (green)
and XSTXST (purple) females (after controlling for thorax length),
in low and high stress food treatments, af ter adjusting for cross.
Points show mean relative eyespan ± one standard error. For
details of the presentation, see Figure 1. Significance values reflect
p- values from Tukey's post hoc comparison tests, ** p < .01

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FINNEGAN Et Al.
quality of the XSR haplotype. Reduced genetic quality is thought
to be typical for low- frequency meiotic drive genes located in or
close to chromosomal inversions or other areas of low recombina-
tion, indicative of weak selection leading to the accumulation of
mutation load (Dyer et al., 2007; Johns et al., 20 05; Larracuente
& Presgraves, 2012; Silver, 1993). There are many examples of vi-
ability and fertility deficits in males and females carrying X- linked
meiotic drive (Curt singer & Feldman, 1980; Dyer et al., 20 07;
Dyer & Hall, 2019; Jaenike, 1996; Larner et al., 2019; Unckless &
Clark, 2014), although it is not known whether these are side ef-
fects of drive itself or due to the accumulation of deleterious muta-
tions at linked loci. In T. dalmanni, a large inversion covers at least a
third and possibly substantially more of the XSR chromosome (Johns
et al., 2005; Reinhardt et al., 2014). The XSR chromosome is esti-
mated to be half a million years old (Paczolt et al., 2017), so there
has been considerable time for mutants to spread and accumulate,
which is reflected in considerable sequence divergence from the
XST chromosome (Reinhardt et al., 2014). Why then is there a lack
of evidence for a condition- dependent deficit in eyespan in males
carrying the XSR haplotype? One possibility arises from the relatively
high frequency of XSR, around 20% in natural populations (Cotton
et al., 2014; Paczolt et al., 2017; Wilkinson et al., 2003). At this fre-
quency, the rate of recombination of XS R is only a quarter of the
standard XST chromosome, and this may be sufficient to allow the
removal of a substantial fraction of deleterious mutations on the XSR
chromosome. Even if this is the case, the XSR chromosome has been
shown to cause a fitness deficit as carriers have reduced egg- to-
adult viability, both in males and in females (Finnegan et al., 2019).
This supports the idea that the XSR haplotype has low genetic quality
and results in reduction of the sexual ornament under low and high
environmental stress. It means that female preference will discrim-
inate against males that carr y the meiotic drive haplotype. But the
low genetic quality of drive males is not reflected in a condition-
dependent expression of the male sexual ornament.
An additional interpretation is that the allocation of limited re-
sources to one trait during development produces compensatory
changes in the relative size of other traits (Nijhout & Emlen, 1998;
Stevens et al., 1999). This hypothesis suggests that the obser ved
pattern of trait size is a reflection of adaptive changes in resource
investment to cope with drive. In SR males, fer tilit y is comparable
to that of ST males despite sperm destruc tion (Meade et al., 2019,
2020). This is accomplished by SR males having greatly enlarged
testes, which allows them to deliver the same number of sperm per
ejaculate as ST males (Meade et al., 2019) and to maintain their fer-
tility even under conditions of multiple mating (Meade et al., 2020),
although there is evidence of fertility loss under an extreme regime
of multiple mating and sperm competition ( Wilkinson et al., 2006).
The alloc ation of increased resources to testes presumably means
that SR males have less to invest in other traits. This may explain
the reduced accessory gland size of SR males, as testes and acces-
sory glands develop over a period of several weeks post- eclosion
(Baker et al., 2003; Meade et al., 2020; Rogers et al., 2008). It is
less obvious why increased investment in testes constrains eyespan
development, as the latter reflects pre- eclosion resource allocation.
However, a mechanistic connection may exist as topical applica-
tion of a juvenile hormone analogue to final instar larvae results in
the development of males with larger testes and smaller eyespan
(Fry, 2006). These observations suggest that larger testes, smaller
eyespan and reduced accessory gland size are outcomes of resource
investment decisions in SR males. One way to test this hypothesis
would be to examine the size of these traits at eclosion. Increased
allocation of resource to testes is predicted to cause a reduction in
allocation to eyespan (which is fixed at eclosion) and the accessory
glands. The resource allocation hypothesis would not be supported
if there was no evidence of increased testes size and decreased ac-
cessory gland size at eclosion, with the dif ference of these reproduc-
tive organs in SR males reflecting post- eclosion development, which
is extensive in stalk- eyed flies, as they only reach sexual maturity
after several weeks of adult life (Baker et al., 2003).
These changes could be adaptive as modelling work shows that
males with fewer resources are expected to produce similar size
ejaculates to those of resource- rich males, but at the expense of
investment in trait s that contribute to the mating rate (Tazzyman
et al., 2009). We have previously shown in stalk- eyed fly SR males
that their larger testes enable them to maintain ejaculate sperm
allocation and fer tility in single and multiple mating, despite drive
causing the loss of half of their sperm (Meade et al., 2019, 2020).
But the smaller eyespan of SR males, independent of environmental
conditions, means they attract fewer females to their lek sites and
hence mate less frequently (Burkhardt & de la Motte, 1988; Cotton
et al., 2010; Hingle et al., 2001; Wilkinson & Reillo, 1994). This may
explain why they have reduced accessory gland size, a trait positively
associated with the mating rate (Rogers et al., 2005). This combina-
tion of investment in traits fits general ideas about life history trade-
offs between secondary sexual traits and ejaculate expenditure
(Simmons et al., 2017), and the specific theoretical prediction that
resources are diverted into maintaining ejaculate size at the expense
of the mating rate (Tazzyman et al., 20 09). Strategic resource invest-
ment likely occurs in a condition- independent manner because drive
is a cellular developmental process disconnected from environmen-
tal stress. This predict s that the strength of drive should be invariant
across environmental stress regimes, which has not yet been explic-
itly tested.
Compensatory responses to meiotic drive that restore organismal
fitness have been investigated previously for resistance mechanisms,
which are highly diverse and widely distributed among species suffer-
ing from both X- linked drive and autosomal drive (Price et al., 2020).
There is also evidence for changes in female polyandr y in systems
where sperm competition impedes the success of sperm from mei-
otic drive males (Manser et al., 2020; Price et al., 2008). In addiiton,
a suite of behavioural and metabolic traits have been hypothesized
to be involved in compensatory mechanisms to t drive in the house
mouse. The t inversion carries recessive lethals, making carrier fitness
negatively frequency- dependent (Runge & Lindholm, 2018). Juvenile
mice carr ying the driving t haplotype show increased dispersal that
could be adaptive if it reduces the likelihood of matings between male

|
7
FINNEGAN E t Al.
and female carriers and consequently the probability of producing ho-
mozygous of fspring (Sutter & Lindholm, 2015). Female carriers of the
t haplotype may additionally compensate for smaller litter size when
they mate with male carriers by having evolved reduced resting met a-
bolic rate (Lopes & Lindholm, 2020). This is associated with extended
lifespan and the production of additional litters in later life (Ferrari
et al., 2019). These l ife history cha nges contrast wi th resistance to d rive
and female polyandry because they enhance the fitness and spread of
the meiotic driver itself (Meade et al., 2020). There are parallels here to
alterations in host behaviour associated with other selfish genetic ele-
ments such as Wolbachia, though it is often unclear whether changes
are detrimental or beneficial to host fitness (Awrahman et al., 2013;
Wedell, 2019). It seems likely that coevolutionary compensation in
host fitness is more common than currently realized.
A further aim of the work here was to examine female eyespan.
This trait shows high condition dependence in stalk- eyed flies,
but to a lesser extent than in the homologous male trait (Cotton
et al., 2004b). We examined eyespan condition dependence in fe-
males and found it was more complex than in males. Under low and
high environmental stress, XSR homozygotes had smaller eyespan
than XST homoz ygotes (though this dif ference was not significant
under high stress; Figures 2– 4). As with males, there was no evidence
for a condition- dependent amplification of genetic differences; the
eyespan dif ference between XSR and XST homoz ygotes was not ex-
aggerated by high environmental stress. The pattern in heterozygous
females was different (Figures 2– 3). Under low stress, heteroz ygotes
were intermediate bet ween the homozygotes. But under high stress,
there was evidence for heterosis as heterozygous females had the
largest eyespan, greater than either homozygote. This heterosis likely
reflec ts the masking of d eleterious allel es (Wilton & Sved, 1979) when
the nonrecombinant and hence highly diverged XSR and XST chromo-
somes are brought together. Our results suggest that heterosis is
dependent on environmental conditions. Under low stress, additive
differences bet ween haplotypes dominate. Under high stress, low
fitness recessive mutations are exposed and the eyespan of homo-
zygotes declines, whereas heterozygotes mask this reduction. As we
do not see an amplification of the difference between homozygous
SR and homozygous ST eyespan, these results do not support the
prediction of a condition- dependent reduction due to the SR hap-
lotype. More work will be necessary to determine whether reduced
homozygous SR female eyespan is the result of strategic resource al-
location, as suggested for males. It would be particularly illuminating
to examine the relationship bet ween drive genotype, eyespan, and
fecundity under varying environmental conditions.
An unforeseen complication in this study arose from the exper-
imental design. In order to collect the full range of male and female
genotypes, two experimental crosses were carried out, Cross A
(XSRXST mated to XSRY) and Cross B (XSRXST mated to XSTY). Larvae
from the two crosses were kept separately throughout egg- adult de-
velopment. Although the rearing conditions of the two crosses were
identic al (larval density, food type, all othe r environmental va riables),
there was a clear effect of cross on female eyespan as heterozygous
female eyespan was larger in Cross A than in Cross B samples. These
heterozygous offspring have the same nuclear genot ype, they share
the same maternal genotype (all heterozygotes), and their mothers
are drawn from the same stock cages and do not differ in maternally
inherited cytot ype. These offspring do differ in paternal genotype
(XSRY in Cross A and XST Y in Cross B), but there is no obvious pa-
ternal effect to explain the difference in eyespan of heterozygous
female offspring. A possible cause is that in Cross A , only female
offspring are produced, whereas in Cross B, the of fspring sex ratio is
approximately 1:1, suggesting that male larvae have a negative com-
petitive effect on female eyespan. This was despite efforts to limit
the amount of competition between larvae by plating a small number
of eggs (12) onto each Petri dish. Differences in male and female
larval competitive abilit y have been reported previously in fruitflies
and mosquitoes (Nunney, 1983; Steinwascher, 2018). In D. melano-
gaster, Nunney (1983) reported that male larvae of some strains were
better at exploiting a limited food supply than females. This was true
even for a strain where females eclosed earlier than males, as is the
case in st alk- eyed flies (unpublished data). In our analysis, we dealt
with this inconsistency by statistically controlling for the effec t of
cross on female eyespan (Figure 3). In addition, a further experiment
was carried out (Figure 4) in which eggs were mixed together from
Cross A (4 eggs) and Cross B (8 eggs). The pair of experiments gave
qualitatively similar results, implying that the statistical adjustment
for the effect of cross was appropriate.
In summar y, meiotic drive causes a reduction in male eyespan,
the sexual ornament in stalk- eyed flies. This occurs under low
and high food stress, in a manner that is not strongly condition-
dependent. A similar reduction is observed in female eyespan, again
across environmental stress levels. But the pattern in females is com-
plicated by heterosis in heterozygotes that is dependent on environ-
mental stress. It seems likely that the reduced eyespan in SR males
reflects contrasting resource allocation to different traits during
FIGURE 4 Absolute female eyespan in low and high stress larval
food treatments in the second experiment when eggs from Cross
A and Cross B were reared together to generate all three female
genotypes: XSRXSR (orange), XSRXST (green), and XSTXST (purple).
Points show mean absolute eyespan ± one standard error. For
details of the presentation, see Figure 1. Significance values reflect
p- values from Tukey's post hoc comparison tests, * p < .05

8
|
FINNEGAN Et Al.
development in order to compensate for the destruction of sperm
caused by meiotic drive.
ACKNOWLEDGMENTS
SRF is supported by a London Natural Environment Research
Council DTP PhD Studentship (NE/L002485/1). AP is supported
by Engineering and Physical Sciences Research Council grants (EP/
F500351/1, EP/I017909/1), and KF and AP by Natural Environment
Research Council grants (NE/G00563X /1, NE/R010579/1). The au-
thors thank Rebecca Finlay and Dr Lara Meade for their help in main-
taining the laboratory stocks and in carrying out the experimental
work.
CONFLICT OF INTEREST
The authors have no conflict of interest to declare.
AUTHOR CONTRIBUTIONS
SRF, KF and AP designed the project and methodology; SRF, KF and
MM collected the data; SRF and MM c arried out the genotyping; and
SRF and AP analysed the data and wrote the paper.
Peer Review
The peer review history for this article is available at https://publo
ns. com/pu blo n/10.1111/ jeb.137 70.
DATA AVAIL ABI LIT Y S TATEM ENT
Data and scripts used in the analyses are available at the Dryad data
depository https://doi.org/10.5061/dryad.x0k6d jhhv
ORCID
Sam Ronan Finnegan https://orcid.org/0000-0001-6893-7068
Kevin Fowler https://orcid.org/0000-0001-9737-7549
Andrew Pomiankowski https://orcid.org/0000-0002-5171-8755
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SUPPORTING INFORMATION
Additional suppor ting information may be found online in the
Supporting Information section.
How to cite this article: Finnegan SR, Mondani M, Fowler K,
Pomiankowski A. Meiotic drive does not cause condition-
dependent reduction of the sexual ornament in stalk- eyed
flies. J Evol Biol. 2021;00:1– 10. https://doi.or g/10.1111/
jeb.13770

J Evol Biol. 2021;00:1–10.
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1wileyonlinelibrary.com/journal/jeb
Received: 25 Septem ber 2020
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Revised: 25 Ja nuary 2021
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Accepted: 27 January 2 021
DOI : 10.1111 /je b.137 70
RESEARCH PAPER
Meiotic drive does not cause condition- dependent reduction of
the sexual ornament in stalk- eyed flies
Sam Ronan Finnegan1 | Matteo Mondani1 | Kevin Fowler1 |
Andrew Pomiankowski1,2
This is an op en access article under t he terms of the Creat ive Commons Attributio n License, which permits use, dist ribution and reproduc tion in any medium,
provide d the orig inal work is proper ly cited .
© 2021 The Authors. Journal of Evolutiona ry Biol ogy published by John Wiley & S ons Ltd on behalf of European So ciety for Evolutio nary Biology.
1Department of Genetics, Evolution and
Environment, University College London,
London, UK
2CoMPLE X, Universit y College London,
London, UK
Correspondence
Andrew Pomiankowski, Department of
Genetics, Evolution and Environment,
University College London, Gowe r Street ,
London WC1E 6BT, UK.
Email: ucbhpom@ucl.ac.uk
Funding information
Engineering and Physical Sciences Research
Council, Grant/Award Number: EP/
F500351/1 and EP/I017909/1; Natural
Environment Research Council, Grant/
Award Number: NE/L002485/1, NE/
G00563X/1 and NE/R010579/1
Graphical Abstract
The contents of this page will be used as part of the graphical abstract of html only.
It will not be published as part of main article.
Malaysian Teleopsis dalmanni stalk- eyed flies carry an X- linked meiotic drive chromo-
some, which reduces eyespan, the male's sexual ornament. Smaller eyespan reflects
compensatory resource allocation and is not a condition- dependent response to the
mutation load on the drive chromosome.