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SEXUAL VS. ASEXUAL REPRODUCTION IN
A STICK INSECT (MEGAPHASMA
DENTRICUS)
Tara Maginnis
University of Portland
Christopher R. Redmond
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(MEGAPHASMA DENTRICUS)" (2016). Biology Faculty Publications and Presentations. 42.
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TEXAS .1. OF SCI. 65(1 ):3-l3
FEBRUARY, 2013 (PUBLISHED JAN 2016)
SEXUAL VS. ASEXUAL REPRODUCTION IN A
STICK INSECT (.MEGAPHASMA DENTRICUS)
Tara M aginnis 1 and Christopher R. Redmond 2
‘Department o f Biology, University o f Portland
5000 N. Willamette Blvd, Portland, OR 97203
2St. Edward's University, Department o f Natural Sciences
3001 S. Congress Ave., Austin, TX 78704
Abstract. -The paradox of sex is one of biology’s great evolutionary questions,
particularly in those species that are fully capable of sexual and asexual reproduction.
To quantify how fitness varies between these two modes of reproduction, we explored
lifetime fecundity in Megaphasma dentricus, the giant walking stick ofNorth America.
For the first 20 days of egg laying, there were no fecundity differences between mated
and unmated females with respect to egg number or egg weight; all females laid a total
of ~50 eggs and each egg weighed about 0.02g. For days 21-50 (the last 30 days of egg
laying), unmated females laid significantly fewer (but not lighter) eggs than sexually
reproducing females. Overall, lifetime fecundity in unmated females was about 5-10%
less than mated females. Myriad factors remain unexplored in this species, including
the ploidy of sexually and asexually produced eggs, the effects of parasites or other
considerations of co-evolution (e.g., the Red Queen Hypothesis), and the accumulation
of deleterious mutations (e.g., Muller’s Ratchet).
Sex is one of evolution’s greatest innovations. However, it is also
one of the most paradoxical, given the ultimate costs of sexual
reproduction (Maynard Smith 1971; Williams 1975; Lloyd 1980;
Michod & Levin 1988; Crow 1994; Misevic et al. 2009; Roze 2012).
For example, sexual reproduction can destroy favorable allelic
combinations during meiosis, and compared to asexual reproduction,
sexually reproducing organisms only contribute half of their genetic
material to offspring. In addition, unmated females who reproduce
asexually may have a higher fitness because they can produce twice
as many offspring compared to sexuals, and thus quickly replace
sexually reproducing individuals (e.g., Maynard Smith’s the “cost of
males” hypothesis, 1978).
Despite potential costs, most animals reproduce sexually. One of
the major evolutionary explanations is genetic variation; given that
an obligate, asexually reproducing population is destined to be a tip
on the tree of life, the reshuffling of genetic material through sex
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helps maintain the raw material for selective processes and potential
speciation (Muller 1964; Felsenstein 1974; Williams 1975; Bell
1982; Otto & Lenormand 2002; Melian et ah, 2012; Song et al.
2012). Two other fundamental hypotheses for the evolution and
persistence o f sexual reproduction include the “Red Queen” and
“Muller’s Ratchet”. Counter to the short-term fitness benefits of
asexual reproduction, clonal populations may be unable to escape
any long-term co-evolutionary pressure that has specialized on their
single genotype (Van Valen 1973; Stenseth 1979; Hamilton et al.
1990; Ridley 1995). For example, in the Red Queen Hypothesis a
population o f genetic clones would be unable to escape a parasite,
leaving the host organism unable to evolve and adapt. Similarly,
without the influx of new, recombinant regions of DNA in each
generation, deleterious mutations cannot be fragmented and are
likely to become fixed in the population. In the long-term this
irreversible (and unidirectional, like a ratchet) accumulation of
maladaptive genetic combinations can drive a clonal population to
extinction (Muller 1932; 1964; Felsenstein 1974).
Although sexual reproduction is the dominant mode of
reproduction in the animal clades, some taxa are capable of both
sexual and asexual reproduction. Walking sticks (Order
Phasmatodea) are fairly unique in that for many species, females can
readily reproduce both sexually and asexually despite a potentially
healthy proportion o f males (Bergerard 1958; Giorgi 1992; Brock
1999; Otte & Brock 2005). Megaphasma dentricus (Stal 1875), the
giant walking stick of North America, is one such species. It lives in
wooded areas of Texas and Oklahoma as well as select regions of
Mexico (Caudell 1903; Arnett 2000; Otte & Brock 2005). Although
field measures o f fecundity are ideal (as there are likely myriad
contributing factors), M. dentricus does not lay eggs in any type of
nest but simply drops them to the ground (prohibiting reasonable data
collection in the field). Thus, through a laboratory investigation we
quantified lifetime fecundity in both mated and unmated M.
dentricus females. Specifically, we aimed to quantify any fecundity
differences in these two modes o f reproduction (measured via egg
MAG1NNIS & REDMOND
5
number and egg weight) to determine if and how asexual
reproduction may be affecting long-term fitness in this species.
M ethods
Thirty adult females and 30 males were collected in Blanco Co.,
TX. Eggs from their sexual copulations were kept at room
temperature in local soil, misted with water bimonthly, and hatched
two years later (e.g., they have a two year incubation, personal
observation). From March-April nymphs were reared together in
large cages (~1 m3) to minimize leg regeneration events due to
molting complications, as investing into leg regrowth can negatively
impact fecundity (see Maginnis 2006; Bely & Nyberg 2010 for
review). Upon their penultimate instar, when the sexes are easily
distinguished (late April), the sexes were separated to ensure
virginity, and individuals with regenerated legs were removed from
the experiment. After maturing (early-mid May), animals were
randomly placed into one of two treatment groups: unmated (females
never exposed to males) or sexual (a monogamous male and female
pair). Although polygyny is common in M. dentricus (Maginnis et al.
2008), we did not have enough individuals to create a third treatment
group with one female and two males.
Animals were kept in 12 L plastic containers covered with
mosquito netting, fed Celtis laevigata {ad libitum), misted with water
daily, and kept in a rooftop greenhouse exposed to natural light and
day cycles. All eggs were collected, counted, and collectively
weighed every day for 50 d between the hours o f 4-7 p.m. 50 d was
chosen as the end point of the experiment for two reasons. First, most
of the females died at day 53 or later (see Results). Second, years of
collecting trips to Blanco County suggest a 30-50 d adult life span;
adults appear in mid-May and can be found in abundance throughout
June, but no individual has been collected past July (Maginnis,
personal observation). Thus, both the lab and the field support 50 d
as a close approximation of lifetime fecundity.
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To look for fecundity differences between mated and unmated
females, we first determined whether or not fecundity was dependent
on body size (measured as both body mass and body length). Periodic
measurements o f female body mass during the first month o f their
reproductive period revealed that weight is extremely variable (as at
any given sampling point females could be unpredictably carrying
one to ten eggs, each weighing -0.02 g) and hence a poor measure of
body size. Thus, for the final analyses, treatment groups were
compared using ANCOVAs with body length as the covariate
(measured from the most anterior part o f the head to the most
posterior portion of the abdomen, not including cerci [see Caudel
1903 for an anatomical reference]). A post-hoc analysis revealed that
mated and unmated females did not significantly differ in body
length (t-te stu n e q u a l variance, P =0.63; X ± S.D. unmated = 111 .8±10.0
mm, mated = 113.4 ± 14.6 mm).
We also determined whether there was a pattern to the number or
weight o f eggs laid per day over the 50 d period, and whether
potential fecundity patterns differed between treatment groups. Two
correlations were done for each female (egg number / over time and
egg weight /over time), and the resulting r-values were compared
across treatment groups with an unpaired t-test assuming unequal
variance. All individual r-values were between -0.41 and 0.03, and
-75% o f the values were between -0.10 and 0.03 (data not shown).
In addition, there were no differences between the treatment groups
for either egg number ( W q u a i variance , P 0.23) or egg weight ( W q u a i
variance —, p ~ 0.27). Since there was no robust pattern to the number
or weight of eggs laid over time, averages were not used for our final
comparisons among treatment groups. Instead, the sum o f egg
number and the sum of egg weight were compared on days 10, 20,
30, 40, and 50. This was done for both individual sets o f 10 d
intervals (e.g., days 1-10, 11-20, 21-30, 31-40, and 41-50) as well as
cumulative sets o f 10 d intervals (e.g., days 1-10, 1-20, 1-30, 1-40,
and 1-50).
MAGINNIS & REDMOND
7
Results
Out of the 52 o f 73 nymphs that survived to maturity, 35 were
used in this experiment; Mmmated = 11 females and AWed = 24 (12
females and 12 males). All other individuals were either used for
breeding stock or were removed from the experiment due to
regeneration (as leg regeneration impacts fecundity). Most of the
females died after day 53, but one unmated female died on day 24,
and one mated female died on day 22. These two females were
analyzed for number and weight o f eggs from days 1-10, 11-20, and
1-20, but were excluded for all other analyses. One male died day 44,
so his female partner was excluded for day 1-50 and 41-50 analyses.
Any individuals still alive by day 63 (N = 9 out of 35) were
euthanized by freezing and included in all analyses.
There were considerable differences between the two treatment
groups with respect to the early and latter periods o f reproduction.
During the first 20 days o f egg laying, there were no fecundity
differences between mated and unmated females (all p > 0.263, see
Tables 1 and 2). However, after day 20, sexually reproducing females
laid more eggs than unmated females (all p < 0.05 except for days
41-50 [p = 0.061], see Tables 1 and 2). There were generally no
differences in egg weight between the early or latter reproduction
periods, or between the two treatment groups (all p > 0.05 except for
days 21-30, see Tables 1 and 2).
D iscussion
The results o f this study suggest that unmated (and thus asexually
reproducing) M. dentricus lay fewer eggs than sexually reproducing
females, but only during the latter period of reproduction. That
unmated females lay fewer eggs than mated females is consistent
with some previous studies on geckos (Kearney & Shine 2005),
salamanders (Uzzel 1964), millipedes (Enghoff 1976), and
planarians (Weinzierl et al. 1999); see Soumalainen (1962) and
Lynch (1984) for early reviews. However, the lack of a fecundity
difference between the two treatment groups during the first 20 days
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Table 1. Cumulative fecundity data for mated and unmated M dentricus
females over the course of 10, 20, 30, 40, and 50 d. (X ± S.D. and
ANCOVA statistics reported).________________________________
unmatcd
mated
unmated
mated
total # o f eggs
total # eggs
total egg w eight (g)
total egg w eight (g)
Days 1-10
23.6 (±9.5)
26.3 (±4.4)
N= 11
N = 12
F ( l , 50) = 0.927 p = 0.347
0.434 (±.18)
0.473 (±.06)
N = 11
N = 12
F ( l , 0.014) = 0.868 p = 0.363
Days 1-20
51.8 (+17.7)
55.2 (±7.2)
N = 11
N = 12
F (1, 126) = 0.893 p = 0.356
0.932 (±0.35)
0.997 (±0.13)
N = 11
N — 12
F ( 1, .057) = 1.325 p = 0.263
Days 1-30
74.6 (±20.6)
83.7 (±8.7)
N = 10
N = 11
F ( l , 693) = 4.539 p = 0.047*
1.373 (±0.50)
1.529 (±0.22)
N = 10
N = 11
F (1,0.257) = 3.235 p = 0.089
Days 1-40
94.1 (±26.6)
109.3 (±14.9)
N = 10
N = 11
F ( l , 1765) = 6,019p = 0.025*
1.764 (±0.67)
2.012 (±0.37)
N = 10
N = 11
F (1,0.589) = 3.538 p = 0.076
Days 1-50
113.2 (±34.5)
134.4 (±19.9)
N = 10
N = 10
F ( l , 2913) = 5.225 p = 0.035*
2.093 (±0.85)
2.504 (±0.47)
N = 10
N = 10
F ( l , 1.192) = 3.835 p = 0.067
Table 2: Fecundity data for individual 10 d periods in mated and unmated M.
dentricus females (X ± S.D. and ANCOVA statistics reported, see Table 1
for Day 1-10 results).
Unmated total #
mated
unmated
mated
o f eggs
total # eggs
total egg w eight (g)
total egg w eight (g)
Days 11-20
28.1 (±13.8)
28.8 (±5.0)
7V= 11
N = 12
F ( 1, 17) = 0.212p = 0.65
0.503 (±0.27)
0.523 (±0.11)
A = 11
N = 12
F ( l , .012) = 0.467p = 0.502
Days 21-30
20.4 (±7.1)
27.5 (±5.1)
N = 10
N = 11
F ( l , 318)= 10.19/7 = 0.005**
.403 (±0.18)
0.520 (±0.13)
N = 10
N = 11
F ( l , .10) = 6.144p = 0.023*
Days 31-40
19.5 (±7.6)
26.0 (±7.7)
N = 10
N = 11
F (1,246) = 4.984 p = 0.039*
0.396 (±0.18)
0.482 (±0.17)
N = 11
N = 10
F (1, .062) = 2.705 p = 0.117
Days 41-50
25.1 (±6.0)
19.1 (±8.7)
N = 10
N = 10
F ( l . 209) = 4.015 p = 0.061
0.354 (±0.19)
0.470 (±0.19)
N = 10
N = 10
F ( l , 0.082) ==3.772 p = 0.069
MAG1NNIS & REDMOND
9
o f their reproductive period is consistent with a related species, the
Vietnamese walking stick (Clitumnus extradentatus, now referred to
as Baculum extradentatum), where unmated females laid just as
many eggs as sexual females for the entire test period of 90 days
(Bergerard 1958). With few studies quantifying the variation
between sexual versus asexual reproduction in phasmids (Lamb &
Willey 1979), if and how M. dentricus and B. extradentatum are
representative o f this diverse groups remains a mystery.
Interestingly, there were generally no differences in egg weight;
regardless of how many eggs each female laid, those eggs were all
approximately the same size. For example, if a mated female lays
135 eggs in her lifetime and they collectively weigh a total o f 2.5 g
(see Days 1-50, Table 1), this means that on average, her eggs
weighed -0.02 g each (2.5 / 135 = 0.0185). Similarly, if an unmated
female lays 113 eggs, collectively weighing 2.1 g (see Days 1-50,
Table 1), her eggs also averaged -0.02 g each (2.1 / 113 = 0.0185).
The one exception to the statistical insignificance between the two
treatment groups was during days 21-30 where eggs from unmated
females were significantly lighter than eggs from mated females. We
have no explanation for these results and/or hypotheses on why there
would be a significant decrease in egg weight for those 10 days.
Regardless, it is likely that stored lipids, proteins, etc. greatly
contribute to egg success over their two-year incubation, so it would
not be surprising if the amount o f resources dedicated to an egg is a
fixed life history trait in this species.
Several additional results from this study are noteworthy. One, the
variation o f unmated female fecundity was much greater than the
variation of mated female fecundity. Especially for the cumulative
fecundity data (see Table 1), the variation o f total egg number and
total egg weight from unmated females was generally double the
variation compared that o f mated females. And two, both egg number
and egg weight tended to decrease of their lifetime, and this was
especially pronounced for unmated females (see Table 2). For
example, while mated females were still producing an average o f 25
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eggs over days 31 -40 and 41-50, unmated females were down to ~20
eggs over those same two time periods. Not surprisingly, this overall
decrease in egg number over time is consistent with the cumulative
fecundity data for the two treatment groups.
Four additional questions remain unanswered and provide a
wealth of future research with M. dentricus. First, what is the ploidy
o f their eggs? Do unmated females lay haploid and/or diploid eggs?
Many phasmid species have shown variation with respect to their
ploidy (Pijnacker 1967; 1969; Marescalchi and Scali 1990; Giorgi
1992; Sandoval et al. 1998; Law and Crespi 2002; Scali et al. 2003;
Ghiselli et al. 2007; Trewick et al. 2008; Schwander and Crespi
2008), and it would be interesting to understand M. dentricus on this
proximate meiotic level. Second, how do considerations of co­
evolution affect the offspring from both mated and unmated females?
(e.g., the Red Queen Hypothesis). In the long-term, clonal and/or
haploid populations may be unable to escape organisms such as
parasites that have specialized on their single genotype. Only studies
that address multiple generations outside of the laboratory setting
will allow us to understand the effects of parasites, predators, and
other selective pressures related to co-evolutionary genetic
phenomena. Third, how quickly do asexually reproducing sub­
populations acquire deleterious mutations? A study by Henry et al.
(2012) found that asexually reproducing female Timema stick insects
had three to 13 fold higher rates of mutations in a suite o f three genes.
That is, for both nuclear and mitochondrial genes the rate of
deleterious mutation accumulation was higher in asexual populations
compared to sexual (Henry et al. 2012). Whether M. dentricus
experiences similar genetic effects is currently unknown but would
prove insightful for the long-term fitness possibilities of wild, clonal
populations. And fourth, does the hatching success of eggs from
mated and unmated females differ? Hobbyists who rear these animals
for recreation have kept female only populations for several years, so
eggs from unmated females are certainly viable (Maginnis, personal
communication). Given that egg weight (a possible predictor of
hatching rate) appears to be a very consistent life history trait in M.
MAGINN1S & REDMOND
11
dentricus, we hypothesize the hatching rates of the eggs produced by
mated and unmated females are similar. This final unanswered
question in M. dentricus is particularly important to understanding
the evolutionary fitness costs of sexual versus asexual reproduction
as Maynard Smith’s “cost of males” only applies if the offspring
produced by asexual reproduction have the same fertility/
hatchability as the offspring produced by sexual reproduction
(Bergerard 1958).
In conclusion, the results from this study suggest that the lifetime
fecundity in unmated females is about 5-10% less than mated
females. However, these differences are driven by the numbers of
eggs laid relatively late in their reproductive period. During the first
twenty days, there were no differences between the total numbers of
eggs laid or the weight o f those eggs, providing no support for the
“cost of males” hypothesis. In fact, these results may be the most
biologically relevant, as in natural populations only a subset of
individuals will survive predation and continue to reproduce after
two or three weeks. Future work that considers ecology as well as
genetics will help our understanding o f the long-term fitness
consequences o f each reproductive strategy.
A cknow ledgem ents
We gratefully thank Andrea Pavia at St. Edward’s University for
assistance in data collection and an anonymous reviewer for helpful
comments on this manuscript. This manuscript is dedicated to the late
Dr. Allan Hook, one of the finest entomologists to set foot in Texas.
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TM at: [email protected]