Journal of Autism and Developmental Disorders (2018) 48:1698–1711

https://doi.org/10.1007/s10803-017-3413-9

ORIGINAL PAPER

What About the Girls? Sex-Based Differences in Autistic Traits

and Adaptive Skills
Allison B. Ratto1,2 · Lauren Kenworthy1 · Benjamin E. Yerys3,4 · Julia Bascom5 · Andrea Trubanova Wieckowski6 ·
Susan W. White6 · Gregory L. Wallace7 · Cara Pugliese1 · Robert T. Schultz3,8 · Thomas H. Ollendick6 · Angela Scarpa6 ·
Sydney Seese1 · Kelly Register‑Brown9 · Alex Martin10 · Laura Gutermuth Anthony1,11

Published online: 4 December 2017

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Abstract
There is growing evidence of a camouflaging effect among females with autism spectrum disorder (ASD), particularly
among those without intellectual disability, which may affect performance on gold-standard diagnostic measures. This study
utilized an age- and IQ-matched sample of school-aged youth (n = 228) diagnosed with ASD to assess sex differences on the
ADOS and ADI-R, parent-reported autistic traits, and adaptive skills. Although females and males were rated similarly on
gold-standard diagnostic measures overall, females with higher IQs were less likely to meet criteria on the ADI-R. Females
were also found to be significantly more impaired on parent reported autistic traits and adaptive skills. Overall, the findings
suggest that some autistic females may be missed by current diagnostic procedures.

Keywords Autism spectrum disorder · Sex differences · Diagnosis · Adaptive skills

Introduction ratio (Fombonne 2009). However, a recent meta-analysis of

epidemiological studies found that the true ratio is likely
Autism spectrum disorder (ASD) is identified in females at a closer to 3:1, with findings suggesting that autistic females1
substantially lower rate than in males, with most epidemio- are more likely to be missed (Loomes et al. 2017). These
logical studies reporting approximately a 4:1 male to female authors and others have hypothesized that autistic traits may

7
* Allison B. Ratto Department of Speech, Language, and Hearing Sciences, The
[email protected] George Washington University, 2115 G St NW, Washington,
DC 20052, USA
1
Center for Autism Spectrum Disorders, Center 8
Departments of Psychiatry and Pediatrics, Perelman School
for Neuroscience Research, Children’s Research Institute,
of Medicine - University of Pennsylvania, 3400 Civic Center
Children’s National Health System, The George Washington
Boulevard, Philadelphia, PA 19104, USA
University School of Medicine, 15245 Shady Grove Rd.,
9
Suite 350, Rockville, MD 20850, USA Department of Psychiatry, University of Maryland School
2 of Medicine, 827 Linden Avenue, Baltimore, MD 21201,
Present Address: Department of Psychiatry, University
USA
of Colorado School of Medicine, Aurora, CO, USA
10
3 Laboratory of Brain and Cognition, National Institute
Center for Autism Research, Children’s Hospital
of Mental Health, Magnuson Clinical Center, Room 4C104,
of Philadelphia, 2716 South Street, Philadelphia, PA 19104,
MSC 1366, Bethesda, MD 20814, USA
USA
11
4 Present Address: Pediatric Mental Health Institute, Children’s
Department of Psychiatry, Perelman School
Hospital of Colorado, Department of Psychiatry, University
of Medicine - University of Pennsylvania, 3400 Civic Center
of Colorado School of Medicine, 13123 East 16th Avenue,
Boulevard, Philadelphia, PA 19104, USA
A036/B130, Aurora, CO 80045, USA
5
Autistic Self Advocacy Network, PO Box 66122,
Washington, DC 20035, USA
6 1
Department of Psychology, Virginia Tech Center for Autism Identity-first language rather than person-first language is used in
Research, Virginia Polytechnic Institute and State University, this manuscript, consistent with practice among autistic self-advo-
3110 Prices Fork Rd., Blacksburg, VA 24060, USA cates (Brown 2011).

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Journal of Autism and Developmental Disorders (2018) 48:1698–1711 1699

be “camouflaged”2 in females and that current diagnostic to be diagnosed with ASD at significantly later ages and to
procedures may be biased against females (Kirkovski et al. experience greater delays in the time from an initial evalu-
2013; Lai et al. 2016). This contrasts strongly to the long- ation to receiving a clinical ASD diagnosis (Begeer et al.
standing belief that females are simply at reduced risk for 2013; Shattuck et al. 2009; Siklos and Kerns 2007). Interest-
developing ASD, based on the consistent finding of lower ingly, data from the Center for Disease Control’s Autism and
prevalence rates among females. Developmental Disabilities Monitoring (ADDM) Network
Studies exploring the etiological basis of ASD have found show that the sex imbalance in diagnostic rates has grown
some support for the observed sex differences in diagnostic over time, from approximately 3.5:1 in 2000 to 4.5:1 in
rates. Many in the field have described a female protective 2010 (Boat and Wu 2015). Although the factors driving this
effect (e.g., Robinson et al. 2013), by which female sex in phenomenon are not yet fully known, it is notable that this
some way directly reduces the risk of ASD. For instance, coincides with a period of time in which rates of ASD have
there is a higher rate of ASD recurrence in families of female been increasing overall, with particular expansion among
probands than in those of male probands, as well as higher children without co-occurring intellectual disability (ID)
rates of autistic traits in the families of female probands (Boat and Wu 2015). It is also well-established that the sex
(Robinson et al. 2013). There are also reports that autis- imbalance in prevalence varies with cognitive ability, with
tic females carry a higher mutational burden, including a a smaller male to female ratio of approximately 2:1 among
higher frequency of both copy number variants (CNVs) and individuals with co-occurring ID and a much larger ratio of
single-nucleotide variants (SNVs) (Gilman et al. 2011; Jac- as much as 6:1 among those with average to above average
quemont et al. 2014). These findings suggest that there may IQ (Fombonne 2009; Kirkovski et al. 2013; Loomes et al.
be a higher genetic threshold for ASD in females relative to 2017; Volkmar et al. 1993). This pattern may indicate that as
males. Hormonal effects have also been hypothesized to play the autism spectrum has expanded to include more individu-
a role in the etiology of ASD and in the observed sex dif- als without co-occurring ID, females in this group have not
ferences in prevalence. Elevated levels of fetal testosterone been adequately identified.
have been implicated in the development of ASD, and there Some prior studies have also found that even when pre-
have been some findings of higher levels of testosterone in senting with comparable levels of socio-communicative
autistic females as compared to typically developing females impairment females are less likely than males to be diag-
(Auyeung et al. 2009; Bejerot et al. 2012; Knickmeyer and nosed with ASD and are more likely to be able to “camou-
Baron-Cohen 2006). Although studies of animal models of flage” their social impairments on performance-based meas-
ASD have not yet placed a strong emphasis on investigat- ures (Dworzynski et al. 2012; Lai et al. 2016; Wilson et al.
ing sex differences, some of these studies have reported 2016). This is particularly true in the case of females without
lower rates of autistic behaviors in female animal models co-occurring ID (Giarelli et al. 2010; Hiller et al. 2016).
as compared to males (e.g., Kataoka et al. 2013; Schoch Qualitative self-report data have also supported the theory
et al. 2017). Although animal models of ASD have obvious that females may be under-diagnosed, as many females who
limitations, these findings are notable, as it would be difficult were diagnosed with ASD late (i.e., in adolescence or adult-
to explain sex differences among animal models as resulting hood) report that they received a series of inaccurate diag-
from camouflaging or diagnostic bias. noses prior to their ASD diagnosis (Bargiela et al. 2016;
Taken together, the etiological literature suggests that Cridland et al. 2014; Trubanova et al. 2014). Given this
it is unlikely that ASD is equally common among males mounting evidence that ASD is not adequately identified in
and females. However, there is growing evidence that cur- females without co-occurring ID, many have theorized that
rent diagnostic procedures may fail to capture the female there may be sex differences in the manifestation of autistic
manifestation of ASD and thus exaggerate the sex imbal- traits in this group, which could in turn contribute to diag-
ance in prevalence rates (Halladay et al. 2015; Kirkovski nostic disparities (Kreiser and White 2014; Lai et al. 2015).
et al. 2013; Loomes et al. 2017). Females have been found Sex differences in the manifestation of autistic traits have
been investigated in a range of studies over the past few
decades. Early work in this field generally found that autistic
2
females were more severely impaired than their male coun-
Researchers and female self-advocates have used the terms “mask-
terparts, presenting with lower IQs and more prominent
ing” and “camouflaging” to describe the phenomenon of autistic
women and girls being missed by current diagnostic procedures. The autistic traits (Lord and Schopler 1985; Lord et al. 1982;
authors chose the term camouflaging, and placed it in quotes for its McLennan et al. 1993; Tsai and Beisler 1983). Subsequent
initial use, to describe this phenomenon which can occur both when studies have found that overall, particularly after control-
autistic women/girls actively seek to hide social communication dif-
ling for IQ, there are not significant differences by sex in
ficulties, as well as when clinicians fail to accurately diagnose them,
due to societal expectations that are believed by many to result in the degree of social-communication impairment, but that
diagnostic bias. restricted/repetitive behaviors (RRBs) are more prominent

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1700 Journal of Autism and Developmental Disorders (2018) 48:1698–1711

in males (Mandy et al. 2012; Pilowsky et al. 1998; Van Wijn- differences among school-age youth in performance on the
gaarden-Cremers et al. 2014; Volkmar et al. 1993). However, gold-standard diagnostic measures: the Autism Diagnostic
important sex differences have been identified in the ways in Observation Schedule (ADOS; Lord et al. 2001) or its recent
which socio-communicative impairments manifest, particu- revision, the ADOS-2 (Lord et al. 2012) and the Autism
larly among those without co-occurring ID. Autistic females Diagnostic Interview-Revised (ADI-R; Rutter et al. 2003),
without ID tend to show more developmentally appropriate which are both widely used to evaluate ASD traits in both
vocabulary and core language skills than their male coun- clinical and research settings. The school-age period (i.e.,
terparts (Halladay et al. 2015; Hiller et al. 2016; Messinger age 6–17) is of critical importance in understanding sex dif-
et al. 2015), though not always (Hartley and Sikora 2009). ferences among those without co-occurring ID, as many of
Given that language delays are the most commonly reported these individuals, particularly females, are first diagnosed
first concern among parents of children with ASD (Chawar- with ASD during this time (Daniels and Mandell 2014; Gia-
ska et al. 2007), this difference may have important implica- relli et al. 2010). Of the studies identified in our literature
tions for diagnostic timing and accuracy. Autistic females review, two reported higher rates of RRBs in males on these
without ID are also more likely to have intact play and imita- measures, consistent with broader findings among autistic
tion skills, which are often considered core impairments in individuals (Bölte et al. 2011; Mandy et al. 2012), while two
ASD (Kirkovski et al. 2013; Knickmeyer et al. 2008; Lord found no sex differences in any of the domains (Holtmann
et al. 1982). Additionally, in contrast to the social isolation et al. 2007; Mandic-Maravic et al. 2015). Due to the field’s
classically described among autistic boys, girls are more heavy reliance on these measures for both clinical diagnosis
likely to be described as “clingy” or overly concerned with and research case ascertainment, understanding sex differ-
being liked by peers (Hiller et al. 2016; Kirkovski et al. ences on these measures is vital, as this may contribute to
2013). Furthermore, some studies have found that parents diagnostic disparities.
rate females as being more socially impaired than their In contrast to the relatively rich literature on sex differ-
male counterparts, even when differences are not apparent ences in autistic traits, fewer studies have focused on sex
on performance-based measures of social-communication differences in adaptive behavior in autistic individuals. It is
skills (Halladay et al. 2015; Holtmann et al. 2007; Kirkovski well-established that autistic individuals have lower adap-
et al. 2013). Additionally, some authors have noted that sex tive behavior than their typically developing peers, and that
differences in RRBs may also be driven by clinician bias, as adaptive skills are often well below expectations based on
females may have restricted interests in more “normative” IQ (Bölte and Poustka 2002; Klin et al. 2007; Pugliese et al.
content areas (e.g., books, celebrities, animals) (Halladay 2015; Volkmar et al. 1987). Furthermore, adaptive behavior
et al. 2015; Kirkovski et al. 2013). It is also worth noting has been shown to be a stronger predictor of overall well-
that prior studies describe patterns of sex differences among being than both autistic traits and IQ, making it a critical
males and females identified by currently available meas- domain in understanding the daily experience of individuals
ures. As described above, the camouflaging effect may mean with ASD (Farley et al. 2009; Kanne et al. 2011). Mixed
that there are some autistic females who are not identified by findings have been reported by the few studies that have
current measures and thus are excluded from these studies. examined sex differences in adaptive behavior, with some
Differences in the manifestation of autistic traits have lent finding that parents rate autistic females as having lower
support to the theory of camouflaging in autistic females, adaptive skills (Carter et al. 2007; Frazier et al. 2014a; Howe
which hypothesizes that females are able to mask socio- et al. 2015), while others find no differences (Andersson
communicative impairments due to increased sensitivity to et al. 2013; Banach et al. 2009; Mandic-Maravic et al. 2015;
social pressure to fit in, gendered expectations for social Reinhardt et al. 2015). Notably, all of these studies have
behavior, and strengths in some social-communication included participants both with and without co-occurring
skills (Lai et al. 2015, 2016). The camouflaging theory has ID/cognitive delay, and many used early childhood samples.
been supported by qualitative interview data from autistic There has not yet been a specific focus on sex differences in
females (Bargiela et al. 2016; Cridland et al. 2014). A recent adaptive behavior among individuals without co-occurring
quantitative study also supported the camouflaging theory, ID, among whom sex differences in autistic traits appear to
finding that autistic females displayed greater discrepancies be strongest.
between clinician-rated and self-rated autistic traits and The goal of the present study was to expand upon prior
core social cognitive abilities, with females showing less research on sex-based differences in autistic traits in indi-
impairment on clinician ratings (Lai et al. 2016). This pat- viduals without co-occurring ID who meet criteria for
tern of findings may indicate that current diagnostic tools ASD on at least one gold-standard diagnostic measure (the
are not as well-suited for evaluating ASD in females and ADOS or ADI-R). We aimed to examine sex differences
may lead to a higher rate of false negatives among females. in autistic traits and adaptive functioning. Based on the
There have been relatively few studies to date examining sex requirement that all participants meet criteria on at least

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Journal of Autism and Developmental Disorders (2018) 48:1698–1711 1701

one gold-standard diagnostic measures, we predicted that on one gold-standard measure may limit the generalizability
our sample would not detect differences in total scores, but of findings and the likelihood of identifying sex differences
that item-level differences would emerge for specific skills. on these measures. The goal of the present study was to
Specifically, we hypothesized that autistic females would focus on sex differences within the population of those with
show significantly lower levels of RRBs than males and bet- ASD who meet criteria commonly used in research to better
ter play and conversation skills than males on performance- understand this targeted population. This limitation will be
based measures, based on prior findings. Consistent with further addressed in the discussion.
the camouflaging theory, we expected that despite similar From the initial sample of 816 participants, a final
performance on gold-standard diagnostic measures, females matched sample of 228 children (n = 114 females) was cre-
would show greater impairments than males in adaptive ated. Participants were matched on full-scale IQ (within five
skills and in parent-report of daily social skills. Further- points) and age (within 1 year) using the case-control match-
more, we hypothesized that sex differences in adaptive skills ing feature (“fuzzy” command) in SPSS 22. The male and
and parent-report of social skills would be reduced among female groups selected by this procedure were not statisti-
participants who met criteria on both the ADOS and ADI-R cally different in age or full-scale IQ, which was assessed
relative to participants who met criteria on only one meas- using a variety of measures, including the Wechsler Abbre-
ure. For this study, we focused specifically on school-age viated Scale of Intelligence (WASI; Wechsler 2011; n = 39),
youth (ages 6–16) who had been evaluated using Module the Wechsler Abbreviated Scale of Intelligence-Second Edi-
3 of the ADOS/ADOS-2 (a play-based and conversation- tion (WASI-II; Wechsler and Hsiao-pin 2011; n = 32), the
based assessment of social communication skills and autistic Wechsler Intelligence Scale for Children-Fourth Edition
traits), as many children without co-occurring ID, particu- (WISC-IV; Wechsler 2003; n = 67), the Wechsler Intelli-
larly girls, are first diagnosed in the school-age period (Dan- gence Scale for Children-Fifth Edition (WISC-V; Wechsler
iels and Mandell 2014; Giarelli et al. 2010). 2014; n = 10), the Wechsler Adult Intelligence Scale-Fourth
Edition (WAIS-IV; Wechsler 2008; n = 1), the Wechsler
Preschool and Primary Scales of Intelligence-Fourth Edi-
Methods tion (WPPSI-IV; Wechsler 2011; n = 1) and the Differen-
tial Ability Scales-Second Edition (DAS-II; Elliot 2007;
Participants n = 78). Average age in the matched sample was 10.11 years
(SD = 2.16; range 6.0–16.25 years); full-scale IQ fell in
Participants were identified from clinic-based and research- the average range overall (M = 101.09, SD = 18.87; range
recruited samples at four different sites across the United 71–145). There were no significant differences in maternal
States: the Center for Autism Spectrum Disorders at Chil- education (χ2 = 5.51, ns) or ethnic distribution (χ2 = 6.48, ns)
dren’s National (Rockville, MD), the National Institute of by sex (see Table 1).
Mental Health Laboratory of Brain and Cognition (Bethesda,
MD), the Center for Autism Research at Children’s Hos- Measures
pital of Philadelphia (Philadelphia, PA) and research and
clinical programs at Virginia Tech, including the Center for Gold‑Standard Diagnostic Measures
Autism Research (Blacksburg, VA). From across these sites,
an initial sample of 816 participants (n = 125 females) was All participants were assessed using Module 3 of the ADOS
identified who had item-level data available on the Module (Lord et al. 2001) or its revision, the ADOS-2 (Lord et al.
3 of the ADOS, a full-scale IQ > 70, and met criteria for 2012). The ADOS is a play-based and conversation-based
ASD based on the following: (1) a diagnosis of ASD from a assessment of social communication skills and autistic traits,
trained clinician based on DSM-IV-TR (American Psychi- designed to be administered by a trained clinician. Module 3
atric Association 2000) and DSM-5 (American Psychiat- of the ADOS is designed for children and adolescents with
ric Association 2013) diagnostic criteria, and (2) met ASD fluent speech. Following administration of the ADOS, the
criteria on the Autism Diagnostic Observation Schedule clinician rates the child on several different behaviors (or
(ADOS; Lord et al. 2012) or its recent revision, the ADOS-2 items), using an ordinal scale, where 0 indicates no evidence
(Lord et al. 2012), and/or the Autism Diagnostic Interview- of impairment, 1 indicates mild impairment, and 2–3 indi-
Revised (ADI-R; Rutter et al. 2003). In this sample, approxi- cates significant impairment. In the most recent version (the
mately 89% (n = 735) participants met criteria on the ADOS/ ADOS-2), scores from selected items are then summed to
ADOS-2, 78% (n = 636) met criteria on the ADI-R, and 70% create a Social Affect score and a restricted/repetitive behav-
(n = 573) met criteria on both measures. As noted above, iors score. These two summary scores are then totaled to
all met criteria on at least one of these two measures. The generate a total algorithm score, which is compared to two
authors recognize that requiring participants to meet criteria cutoff scores: one for “Autism” and another for “Autism

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1702 Journal of Autism and Developmental Disorders (2018) 48:1698–1711

Table 1  Demographics
Males (N = 114) Females (N = 114) Statistic, p value

Maternal education χ2 = 5.51 (ns)

Graduate degree 38 35
College degree 30 34
Associate’s degree/partial college 19 7
High school diploma 5 5
Partial high school 5 3
Other/unknown 17 30
Race χ2 = 6.48 (ns)
White 88 79
Black 4 12
Asian 3 7
Latino/a 6 6
Other/unknown 13 10
Age 10.12 (2.15) 10.11 (2.19) t = 0.025 (ns)
Full-scale IQ (mean/SD) 101.03 (18.67) 101.16 (19.14) t = − 0.053 (ns)
ADOS-2 (N) 114 114
ADOS-2: overall (mean/SD) 13.40 (5.51) 12.60 (4.97) n/a
ADOS-2: social affect (mean/SD) 10.07 (4.57) 9.76 (4.27) n/a
ADOS-2: restricted/repetitive behavior (mean/SD) 3.33 (2.13) 2.83 (1.88) n/a
ADOS-2: comparison score (mean/SD) 7.37 (1.98) 7.14 (2.17) 0.830 (ns)
ADI-R (N) 99 96
ADI-R: reciprocal social interaction (mean/SD) 17.79 (5.82) 17.86 (5.54) n/a
ADI-R: communication (mean/SD) 14.90 (4.46) 14.94 (4.81) n/a
ADI-R: restricted/repetitive behavior (mean/SD) 5.55 (2.32) 5.50 (2.66) n/a

Spectrum.” Although one new item was added to the Module and Abnormalities of Development at or before 36 months.
3 in the ADOS-2, this new item was not included in the total For the present study, the algorithm scores based on his-
algorithm, and thus all participants were compared using the torical information (i.e., behaviors between ages 4–5 years)
ADOS-2 algorithm, regardless of the version of the ADOS were used because these scores have been determined to
that was administered. Participants were considered to have best discriminate ASD from non-ASD (Boelte and Poustka
met research criteria for ASD on the ADOS/ADOS-2 if their 2000). Participants are considered to have met criteria for
score was at or above the “Autism Spectrum” cutoff of 7. In ASD on the ADI-R if their algorithm scores meet or exceed
addition to the diagnostic algorithm, the ADOS-2 also calcu- cutoff criteria in each of the four domains.
lates a Comparison Score, which provides a severity ranking
of 1–10 (1: minimal-to-no evidence, 10: high) based on the Parent‑Reported ASD Traits
individual’s diagnostic algorithm score and age.
The Autism Diagnostic Interview-Revised (ADI-R; Rut- The Social Responsiveness Scale (SRS; Constantino and
ter et al. 2003) is a semi-structured diagnostic interview, Gruber 2005), and its update the Social Responsiveness
designed to be administered by a trained clinician with a par- Scale-2 (SRS-2; Constantino and Gruber 2012), are sex-
ent or caregiver. The ADI-R gathers information on both cur- normed parent-report measures of autistic traits for children
rent and historical functioning, focusing on the year between ages 4–18. Parents rate their children on several different
the child’s fourth and fifth birthdays. Parent responses to behaviors, using a Likert scale of 1–4. T-scores are gener-
items asking about specific ASD traits are coded on an ated within five domains of ASD traits: social awareness,
ordinal scale that parallels the ADOS, where 0 indicates social cognition, social motivation, social communication,
no evidence of impairment, 1 indicates mild impairment, and restricted/repetitive behaviors, as well as a total score,
and 2–3 indicates significant impairment. Scores for selected where higher scores indicate higher levels of autistic traits.
items are then summed to create algorithm scores for four
domains: Reciprocal social interaction, communication,
Restricted, Repetitive, and Stereotyped Patterns of Behavior,

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Parent‑Reported Adaptive Behavior Results

Adaptive behavior was assessed using the Vineland Adap- Sex Differences on Gold‑Standard Diagnostic
tive Behavior Scales, Second Edition, Survey Interview Measures
(Vineland-II; Sparrow et al. 2005). The Vineland-II is a
sex-normed and age-normed measure that assesses adap- Overall, approximately 90% of females and 94% of males
tive behavior skills in individuals from birth to age 90 and in this sample met “Autism Spectrum” cutoff criteria on
divides adaptive behavior into three broad domains in this the ADOS/ADOS-2, using the ADOS-2 diagnostic algo-
age group: communication skills, daily living skills, and rithm (Pearson χ2 = 0.965, ns; Table 1). Consistent with our
social skills. Standard scores are generated for each domain, hypotheses, there were no significant sex differences in the
as well as for the adaptive behavior composite (ABC). ADOS-2 Comparison Score (t = 0.830, ns; Table 1), indi-
cating similar levels of overall autistic traits across sexes.
Data Analysis Similarly, there were no significant differences in likeli-
hood of meeting ASD criteria on the ADI-R by sex (Pearson
Item-level data were available for all participants on the χ2 = 0.208, ns), with 72.63% of females (n = 69) and 75.51%
ADOS. Complete data (i.e., domain scores) were available (n = 74) of males meeting criteria. Performance on gold-
for 85% (n = 193 total, n = 95 females) of the matched sam- standard measures was further explored through item-level
ple on the ADI-R, for 80% (n = 182 total, n = 91 females) of analyses of the ADOS. Consistent with our hypotheses,
the sample on the SRS, and for 76% (n = 174 total, n = 77 females showed less evidence of RRBs, as evidenced by
females) of the sample on the Vineland-II. Individuals for lower scores on the Excessive Interests item of the ADOS
whom the data were not available on particular measures (Pearson χ2 = 5.799, p = .055), with a small effect size
were excluded from those specific analyses, such that the (Φ = 0.159). Contrary to hypotheses, no significant sex dif-
samples for these analyses were not statistically matched. ferences were found in play skills (Imagination/Creativity,
However, there were still no statistical differences in age (p Pearson χ2 = 0.971, ns) or conversation skills (Conversa-
values range .267–.624) or IQ (p values range .495–.916) by tion, Pearson χ2 = 2.483, ns) on the ADOS. Females were
sex among these reduced samples. To evaluate our hypoth- less likely to direct a range of facial expressions towards the
esis that males and females would show similar levels of examiner during the ADOS (Facial Expressions, Pearson
ASD traits on gold-standard measures by sex, Pearson Chi χ2 = 9.049, p = .01), with a small effect size (Φ = 0.199). At
square analyses were used to assess sex differences in rates the trend level, females out-performed males in identify-
of meeting ASD criteria on the ADOS and the ADI-R, and t ing and sharing emotions with others (Empathy, Pearson
tests were used to assess sex differences in the ADOS Com- χ2 = 4.754, p = .09), with a small effect size (Φ = 0.144), and
parison Score (an indicator of number of ASD traits). Pear- showed lower rates of hyperactivity (Overactivity, Pearson
son Chi square analyses of item-level data on the ADOS χ2 = 5.535, p = .063), with a small effect size (Φ = 0.156).
were used to evaluate the hypothesis that females would However, none of these findings survived corrections for
show fewer RRBs and better conversation and play skills multiple comparisons, indicating that overall, performance
than males. Additional exploratory analyses using Pear- on the ADOS was similar between males and females.
son chi-squares were then undertaken to investigate other Due to the unexpected finding of a relatively low percent-
potential sex differences in item-level performance on the age of participants overall meeting ASD cutoff criteria on
ADOS. Effect sizes for Chi square analyses were calculated ADI-R (74.09%, n = 143 of 193 available), post-hoc analy-
using Cramer’s phi (Φ) coefficient; by convention, Φ = 0.10 ses were undertaken to further explore this finding. Among
is interpreted as a small effect size, Φ = 0.30 as a medium the 193 participants who received the ADI-R, sociodemo-
effect size, and Φ = 0.50 is considered a large effect (Cohen graphic characteristics were consistent with the full sample.
1988). One-way ANOVAs were used to analyze differences Logistic regression was used to determine whether domain
by sex in scores on both the SRS and the Vineland-II, evalu- scores related differentially to likelihood of meeting criteria
ating the hypothesis that females would show greater levels on the ADI-R, with meeting ASD criteria on the ADI-R as
of parent-reported difficulty with social and adaptive skills. the binary outcome, and scores on each of the four domains
Two-way ANOVAs were used to assess the hypothesis that (reciprocal social interaction, communication, restricted/
participants who met diagnostic criteria on both the ADOS repetitive behaviors, early developmental abnormalities) as
and ADI-R would show fewer sex differences than partici- the predictors. To meet criteria on the ADI-R algorithm,
pants meeting on only one measure (the ADOS). Effect sizes an individual must obtain a score of 10 out of 30 possible
for ANOVAs were calculated using Cohen’s d. The false points on the Reciprocal Social Interaction domain (33%),
discovery rate procedure (Benjamini and Hochberg 1995) 8 out of 26 on the communication domain (31%), 3 out of
was used to control for Type I error rate in all analyses.

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1704 Journal of Autism and Developmental Disorders (2018) 48:1698–1711

Table 2  Logistic regression of Autism Diagnostic Interview-Revised predictor. When this analysis was re-conducted separately
Β Wald criterion p value Exp. (β)
by sex, Early Developmental Abnormalities was the only
domain to significantly predict meeting ADI-R criteria over-
Total sample all among females. Among males, the communication and
Reciprocal social interac- 0.107 4.787 .029 1.113 restricted/repetitive behaviors domains were both significant
tion
predictors of meeting ADI-R criteria.
Communication 0.105 2.683 .101 1.111
Because early developmental delays are predictive of later
Restricted/repetitive 0.229 6.961 .008 1.258
behavior
intellectual ability, and this domain emerged as a key pre-
Abnormal development 0.464 9.215 .002 1.591
dictor for females, an additional exploratory analysis was
Females only
conducted to examine whether IQ at the time of the ADOS
Reciprocal social inter- 0.114 2.311 .128 1.121
related to likelihood of meeting criteria on the ADI-R. A
action hierarchical logistic regression was performed to predict
Communication 0.030 0.112 .738 1.030 meeting ADI-R criteria, with all four ADI-R domain scores
Restricted/repetitive 0.178 2.889 .089 1.195 entered in the first block, and sex, full-scale IQ, and the
behavior interaction of sex and IQ in the next block. After accounting
Abnormal development 0.515 6.597 .010 1.673 for the effects of domain scores, sex significantly predicted
Males only likelihood of meeting criteria on the ADI-R (β = − 4.46,
Reciprocal social inter- 0.125 3.182 .074 1.133 Wald criterion = 3.82, p = .051), such that females were sig-
action nificantly less likely to meet criteria. The interaction of sex
Communication 0.208 4.323 .038 1.232 and IQ was also significant (β = 0.041, Wald criterion = 3.58,
Restricted/repetitive 0.289 3.659 .056 1.335 p = .058), such that females with higher IQs were the least
behavior
likely to meet criteria on the ADI-R.
Abnormal development 0.405 2.585 .108 1.499

Parent Report of Daily Functioning

12 on the restricted/repetitive behaviors domain (25%) and 1 One-way ANOVAs revealed significant differences on all
out of 5 on the Early Developmental Abnormalities domain five domains of the SRS. Females were rated as having sig-
(20%). Thus, although the point totals differ by domain, nificantly stronger autistic traits across all domains, with
the proportion of points required to pass each domain is effect sizes ranging from small to large (Table 3; Fig. 1). On
roughly equal, with the Early Developmental Abnormalities the Vineland-II, one-way ANOVAs (Table 3; Fig. 2) revealed
domain as the “easiest” criterion to pass by proportion. In that females had significantly lower daily living skills [F
the full sample, all domain scores were significant predic- (1,172) = 4.77, p = .03] than males, with a small effect size
tors of meeting criteria on the ADI-R, as expected, with the (Cohen’s d = 0.335). Social skills were also more impaired
exception of the communication domain (Table 2). Early in females, at the trend level [F (1,172) = 2.93, p = .09]. No
Developmental Abnormalities were the strongest overall significant differences were found for communication skills.

Table 3  Parent report of daily functioning

Social Responsiveness Scale (T-scores) Males Females F (1,180)/p value Cohen’s d
M (SD) M (SD)
N = 91 N = 91

Social awareness 67.92 (13.64) 75.24 (12.32) 14.425 (p = .0001) 0.566

Social cognition 73.63 (13.05) 80.01 (13.58) 10.451 (p = .001) 0.482
Social communication 73.87 (12.72) 83.41 (13.56) 23.958 (p = .0001) 0.730
Social motivation 68.91 (13.93) 74.04 (14.93) 5.745 (p = .02) 0.357
Autistic mannerisms/RRBs 77.92 (15.85) 88.40 (17.51) 17.895 (p = .0001) 0.631
Vineland Adaptive Behavior Scales-II (standard Males Females F (1, 172)/p value Cohen’s d
scores) M (SD) M (SD)
N = 97 N = 77

Communication 83.58 (14.04) 81.95 (14.47) 0.563 (ns) 0.115

Daily living 81.93 (14.13) 77.13 (14.70) 4.77 (p = .03) 0.335
Socialization 75.94 (14.70) 72.31 (12.59) 2.93 (p = .09) 0.263

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Journal of Autism and Developmental Disorders (2018) 48:1698–1711 1705

Fig. 1  Sex differences in 100

parent-reported autistic traits 88.4
90 83.41
on the Social Responsiveness 80.01 77.92
80 75.24 73.63 73.87 74.04
Scale. Note: results shown with 68.91
67.92
standard error bars 70

SRS T-scores
60
50
40
30
20
10
0
Social Awareness Social Cognition Social Social Motivation RRBs
Communication
Males Females

Fig. 2  Sex differences in parent- 100

reported adaptive functioning 83.58
90 81.95 81.93
on the Vineland-II Adaptive 75.94
77.13
Vineland-II Standard Scores

Behavior Scales. Note: results 80 72.31

shown with standard error bars 70
60
50
40
30
20
10
0
Communication Daily Living Socialization
Males Females

All findings on the SRS-2 retained significance after control- used, based on the average age of participants. The SRS is
ling for multiple comparisons, as well as the differences on not age-normed. The raw score associated with the mean
the Vineland-II daily living scale. Since both the SRS and score for females was higher across all subscales of the SRS
the Vineland-II are sex-normed measures, this pattern of and lower across all subscales of the Vineland-II, consistent
findings indicates that autistic females were rated as more with hypotheses.
impaired with respect to typically developing females than To assess the hypothesis that participants who met diag-
autistic males were when compared to typically develop- nostic criteria on both the ADOS and the ADI-R would show
ing males. Raw score data were not available for all partici- fewer sex differences than those meeting criteria on only
pants to assess whether the significant difference in normed one measure, participants who had received both measures
scores corresponded to a significant difference in raw scores (n = 193) were then divided into three groups, based on
as well, which would indicate that autistic females showed whether they met diagnostic criteria on ADOS only (n = 22
stronger autistic traits and greater adaptive impairments than males, 23 females), on ADI-R only (n = 2 males, 8 females),
autistic males. However, when the sample mean was com- or on both measures (n = 72 males, 62 females). This distri-
pared to the normative tables to determine the corresponding bution did not differ significantly by sex (Pearson χ2 = 4.322,
raw score for each scale, the female raw score was consist- p = .115). Given the very small number of participants who
ently higher across all subscales (Table 4). Although stand- met criteria on the ADI-R only, further analyses focused on
ard deviations could not be calculated to examine this statis- comparison of those who met on ADOS only versus those
tically, this pattern of findings is consistent with hypotheses who met on both measures. Two-way ANOVAs were used to
that autistic females would show stronger autistic traits and analyze the effects of sex and number of measures on which
greater adaptive skill impairments than autistic males. For ASD criteria were met (i.e., both the ADOS and ADI-R ver-
the Vineland-II, the normative table for ages 10:0–10:11 was sus the ADOS alone) on parent-reported functioning. For

13
1706 Journal of Autism and Developmental Disorders (2018) 48:1698–1711

Table 4  Raw scores corresponding to sample means by sex

Social Responsiveness Scale Males T-score mean Males corresponding raw Females T-score mean Females cor-
score responding raw
score

Social awareness 67.92 11 75.24 13

Social cognition 73.63 19 80.01 21
Social communication 73.87 33 83.41 38
Social motivation 68.91 15 74.04 16
Autistic mannerisms/RRBs 77.92 21 88.40 23
Vineland Adaptive Behavior Scales-II Males standard score Males corresponding raw Females standard score Females cor-
mean score mean responding raw
score

Communication 83.58 37 81.95 36

Daily living 81.93 37 77.13 34
Socialization 75.94 32 72.31 30

Determination of raw scores was performed by rounding T-scores and standard scores to nearest whole number, following usual conventions
(< 0.5: round down, > 0.5: round up). When the exact T-score mean did not appear in the normative table, the nearest T-score below the rounded
mean was used and the nearest Standard Score above the mean was used, for conservative estimation (i.e. assuming weaker autistic traits and
higher adaptive skills)

Table 5  Two-way ANOVAs of parent-reported daily functioning by sex and diagnostic criteria met
Main effect of sex Main effect of diagnostic criteria Interaction effect
(ADOS only vs. ADOS + ADI-R)

Social Responsiveness Scale

Social awareness F (1,143) = 10.166, p = .002 F (1,143) = 1.089, ns F (1,143) = 0.011, ns
Social cognition F (1,143) = 9.382, p = .003 F (1,143) = 2.910, p = .090 F (1,143) = 0.262, ns
Social communication F (1,143) = 12.634, p = .001 F (1,143) = 1.870, ns F (1,143) = 0.649, ns
Social motivation F (1,143) = 1.507, ns F (1,143) = 0.676, ns F (1,143) = 0.936, ns
Autistic mannerisms/RRB F (1,143) = 6.774, p = .010 F (1,143) = 4.732, p = .031 F (1,143) = 1.171, ns
Vineland-II
Communication F (1,138) = 1.581, ns F (1,138) = 3.249, ns F (1,138) = 0.360, ns
Daily living F (1,138) = 3.118, p = .080 F (1,138) = 4.182, p = .043 F (1,138) = 0.157, ns
Socialization F (1,138) = 5.291, p = .023 F (1,138) = 1.609, ns F (1,138) = 3.070, p = .082

the SRS, results were largely consistent with results of the not significant. On the Social domain, there was a significant
one-way ANOVAs (Table 4). There was a main effect of main effect of sex, such that females had lower skills on
sex on all domains of the SRS, with the exception of social average. The main effect of meeting ASD criteria on one
motivation. The effects of meeting criteria on one versus versus two measures was not significant; however, there was
two measures were significant for the restricted/repetitive an interaction effect at the trend level, such that there were
behaviors domain and at the trend level for the Social Cog- greater sex differences among those who met on the ADOS
nition domain, such that participants who met criteria on only, consistent with our hypotheses. On the communication
both measures were rated as having stronger autistic traits in domain, there was a trend-level effect of meeting criteria on
these domains. There were no significant interaction effects one versus two measures, such that participants who met on
on any items. On the Vineland-II, results were also generally both measures showed greater impairments. The main effect
consistent with the one-way ANOVAs. For the daily living of sex and the interaction effect were both non-significant.
skills domain, there was a significant main effect of meeting Again, controlling for multiple comparisons retained all
criteria on one versus two measures, such that participants significant findings on both the SRS and the Vineland-II
who met on both the ADOS and the ADI-R had lower skills (Table 5).
on average. There was also a main effect of sex at the trend
level, with females showing lower skills. The interaction was

13
Journal of Autism and Developmental Disorders (2018) 48:1698–1711 1707

Discussion not uniquely indicative of stronger autistic traits, but rather

of greater clinical impairment overall.
This study was the first investigation of sex differences in The findings also raise questions about the sensitivity of
both adaptive behavior and daily social skills among school- gold standard autism diagnostic tools for females. A notable
age youth diagnosed with ASD without co-occurring ID. minority of this sample failed to meet diagnostic criteria
Results supported our hypotheses, based on the camouflag- on the ADI-R, despite meeting ASD criteria on both the
ing theory, that autistic females would be more impaired ADOS-2 algorithm and in the judgment of an experienced
on parent-reported measures of adaptive behavior and daily clinician. Females with higher cognitive ability were at the
social functioning, despite similar overall performance on greatest risk of failing to meet ADI-R criteria. Notably, anal-
gold-standard diagnostic measures. Females were rated as yses revealed that a failure to show early developmental dif-
having stronger autistic traits by their parents than their male ferences was the strongest predictor of failing to meet ADI-R
counterparts in comparison to their typically developing criteria in the sample, particularly among females, and that
peers. Additionally, autistic females were rated as having this was particularly true for females with higher intellectual
lower daily living skills than autistic males, when compared ability. This result raises concerns that individuals without
to a normative sample. Although statistical analysis of raw ID of both sexes, but particularly females, may not receive
scores was not possible, corresponding raw score data were accurate clinical diagnoses and may also be unnecessarily
also indicative of stronger autistic traits and lower daily liv- excluded from research trials if inclusion criteria are tightly
ing skills among autistic females than autistic males. Over- tethered to exceeding threshold on these standardized tools.
all, this pattern of findings suggests that the females who Of note, early developmental delays have been removed
ultimately met criteria on gold-standard diagnostic measures from the clinical diagnostic criteria for ASD in the DSM-
were more severely affected in real-world settings than their 5; the diagnostic algorithm of the ADI-R may also need to
male counterparts. This may be an indication that females be updated to be consistent with the DSM-5. Moreover, if
required a stronger manifestation of autistic traits in order the females in this sample represent only the girls with the
to meet criteria on gold-standard measures. However, it is strongest autistic traits, this necessarily raises the question
also possible that parents respond to these measures dif- of whether there are girls with less intense autistic traits who
ferently when reporting about their daughters as compared may not meet strict cutoff criteria on gold-standard meas-
to their sons. Parents may expect girls to be more socially ures, but who nonetheless meet DSM-5 criteria for ASD.
competent, for example, and thus see their daughters as more The variability in the sex ratio in ASD by cognitive ability,
impaired by social differences due to their higher expecta- from 2:1 among those with ID to as high as 6:1 among those
tions. However, this possibility seems less likely, given that without ID, also raises the question of whether females with
both the Vineland-II and the SRS are sex-normed, and thus higher cognitive abilities may be missed, consistent with the
should already account for societal differences in parental findings in the present sample that females were less likely
expectations. It is also notable that both the Vineland-II and to meet ADI-R criteria as intellectual ability increased.
the SRS are sex-normed measures, using continuous rating There is no clear theoretical reason why the female protec-
scales, while the ADOS and ADI-R are best conceptual- tive effect would be stronger as cognitive ability increases,
ized as symptom-count measures, which were developed and thus it seems likely that current diagnostic procedures
on predominantly male samples without sex-specific cutoffs fail to adequately identify females with higher intellectual
or algorithms. The use of sex norms likely makes the SRS abilities. There are indications that this disparity impacts
and the Vineland more sensitive to possible sex differences. even early screening procedures, as prior studies have found
Additionally, the use of the continuous rating scale in the that parents’ first concerns differ by sex (Hiller et al. 2016;
SRS, as opposed to the ordinal scale of the ADOS, allows for Little et al. 2016), and at least one recent study has found sex
greater variability in scores, and potentially a stronger ability differences at the item-level on the Modified Checklist for
to capture more subtle sex-based differences in the intensity Autism in Toddlers (M-CHAT), one of the most widely-used
of autistic traits. However, the findings on the separate sub- early ASD screening instruments (Øien et al. 2017).
scales of the SRS should be interpreted with some caution, The findings in this study provide an initial indication
as there is stronger support for the two-factor structure in the of potential sex differences in the profile of autistic traits;
SRS-2 (social-communication index and restricted/repetitive however, additional research is needed to further investi-
behaviors scale) than for the five-factor structure utilized gate the manifestation and experience of ASD across the
in both the SRS and SRS-2 (Frazier et al. 2014b). There gender spectrum. Further evaluation of the camouflaging
are also indications that non-ASD clinical samples may also hypothesis is also needed to understand if this is an impor-
have elevated scores on the SRS (Pine et al. 2008; Yerys tant factor in explaining sex differences in diagnostic rates.
et al. 2009), and thus it is possible that these findings are Cognitive interviewing techniques (Beatty and Willis 2007)
are a well-established methodology for gathering additional

13
1708 Journal of Autism and Developmental Disorders (2018) 48:1698–1711

information from participants about how they understand often able to mask their autistic traits, and thus are never
and respond to psychological surveys and measures. Use of identified and never receive appropriate supports. A broader
cognitive interviewing with the ADOS will allow research- sampling of autistic females, who may not meet criteria on
ers to explore and better understand the ways in which autis- gold-standard measures but do meet DSM-5 criteria, would
tic individuals experience the ADOS, as well as how well likely yield greater sex differences. We assert that the over-
they feel the ADOS captures their daily social functioning. reliance on these measures in research trials, including in
This type of structured, qualitative data provides valuable the present study, creates a self-perpetuating cycle, by which
information to guide our understanding of the effectiveness females whose autistic traits may not align with the ADOS
of our measures with this population, which may not be well and ADI-R, or who may be able to “pass” an ADOS, are
characterized currently. It will also be important to explore excluded from research. Researchers then fail to find sex
diagnostic pathways in future research. As described above, differences in their studies because the very females who we
autistic females have been found to be vulnerable to inac- are most interested in studying cannot be included. While
curate and delayed diagnoses. Researchers have begun pay- the ADOS and ADI-R are powerful tools, strict adherence
ing increased attention to female self-advocates, who have to these measures as the only acceptable way of validating
described their experiences of being misdiagnosed for sev- an ASD diagnosis inherently restricts our research samples
eral years prior to obtaining a diagnosis of ASD, and the del- and limits our ability to understand sex differences in ASD.
eterious effects that inappropriate behavioral, educational, Because research informs clinical practice, this emphasis
and psychiatric treatments have had on their lives (Bargiela on the ADOS/ADI-R may also lead to an over-reliance on
et al. 2016). We need more information about the inaccurate these measures among clinicians, such that females who do
diagnoses that autistic females most often receive prior to not meet criteria on these measures are never diagnosed, and
being accurately diagnosed, as well as information about thus do not gain access to valuable services and appropri-
how they are ultimately able to obtain a diagnosis of ASD, in ate interventions. Innovative methodologies are needed to
order to understand the limitations of our current diagnostic develop reliable and valid methods of accurately identifying
methodologies and pathways to treatment. It will also be these autistic girls and women to enable access to needed
important to evaluate sex differences in other age groups, clinical services and participation in research.
particularly at younger ages, in light of the ADI-R findings It should also be noted that this study investigated sex-
in this sample. Longitudinal studies on children who even- based differences in ASD, as defined by biological sex
tually develop ASD, who develop other clinical conditions assigned at birth. However, there are higher rates of gen-
(e.g., ADHD, anxiety), and of typically developing children der variance in autistic individuals (Strang et al. 2014).
are also needed to study developmental pathways over time, Although biological sex traits may drive differences in the
to understand when and how males and females begin to manifestation of autistic traits, gender identity will almost
manifest autistic traits differently. Longitudinal studies could certainly influence the manifestation of autistic traits as well.
also provide prospective data on the potential effects of later Future research needs to consider not only sex-based differ-
diagnosis on females’ development and well-being (e.g., ences, but also the role that gender identity, including gender
missed opportunities for early intervention and supports). non-conformity, may play in the manifestation of ASD.
This study was limited, as are most studies in the field, by
its reliance on the ADOS and ADI-R for case ascertainment. Acknowledgments Funding for this project was provided by grants
and financial support through several institutions, including: The Isa-
Some authors investigating sex differences have noted that dore and Bertha Gudelsky Family Foundation, Children’s National
using stringent cutoff scores on standardized measures as Health Institute IDDRC P30 HD040677, Pennsylvania State Depart-
inclusion criteria may overly restrict our samples, limiting ment of Health, The Philadelphia Foundation, Pfizer, Robert Wood
our ability to capture true sex differences in the manifes- Johnson Foundation, Virginia Tech Center for Autism Research,
and the National Institute of Child Health and Human Development
tation of ASD (e.g., Lai et al. 2016). Having been devel- (R03HD081070). We are grateful to the children and families who
oped with a predominantly male sample, the ADOS and the participated in this study.
ADI-R likely are best at capturing autistic traits as they are
most commonly manifested in males. Thus, females cur- Author Contributions ABR collected the data, ran the analyses, and
rently included in studies like this one may be those with wrote the paper. LK served as co-principal investigator for one site of
the project, collected the data, helped design the analyses, and wrote
autistic trait profiles that are closest to the prototypical male the paper. BEY served as co-principal investigator for one site of the
profile of ASD. Autistic females who show a different pat- project, collected the data, provided feedback on analyses, and wrote
tern of autistic traits or who evidence less readily apparent the paper. JB provided insight and feedback on the interpretation of
socio-communicative impairments may not be appropriately analyses and edited the paper. ATW collected the data and edited the
paper. SWW served as co-principal investigator for one site of the pro-
captured by currently available diagnostic tools. It is quite ject, collected the data, provided feedback on analyses, and edited the
possible that there exists a group of autistic females who do paper. GLW collected the data, helped design the analyses, and edited
not fit the “classic” (i.e., male) profile of ASD, and who are the paper. CP collected the data, provided feedback on analyses, and

13
Journal of Autism and Developmental Disorders (2018) 48:1698–1711 1709

wrote the paper. RTS collected the data, provided feedback on analyses, Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discov-
and edited the paper. THO collected the data, provided feedback on ery rate: A practical and powerful approach to multiple testing.
analyses, and edited the paper. AS collected the data, provided feed- Journal of the Royal Statistical Society. Series B, 57(1), 289–300.
back on analyses, and edited the paper. SS collected the data, managed Retrieved from http://www.jstor.org/stable/2346101.
the database, and edited the paper. KR-B provided feedback on analyses Boat, T. F., & Wu, J. T. (Eds.). (2015). Prevalence of autism spectrum
and edited the paper. AM served as co-principal investigator for one disorder. In Mental disorders and disabilities among low-income
site of the project, collected the data, provided feedback on analyses, children (pp. 241–266). Washington, DC: The National Acad-
and edited the paper. LGA served as co-principal investigator for one emies Press.
site of the project, collected the data, helped design the analyses, and Boelte, S., & Poustka, F. (2000). Diagnosis of autism: The connec-
edited the paper. tion between current and historical information. Autism, 4(4),
382–390. https://doi.org/10.1177/1362361300004004004.
Bölte, S., Duketis, E., Poustka, F., & Holtmann, M. (2011). Sex differ-
Compliance with Ethical Standards ences in cognitive domains and their clinical correlates in higher-
functioning autism spectrum disorders. Autism, 15(4), 497–511.
Conflict of interest All authors declare no conflict of interest. https://doi.org/10.1177/1362361310391116.
Bölte, S., & Poustka, F. (2002). The relation between general cognitive
Ethical Approval All procedures performed in studies involving level and adaptive behavior domains in individuals with autism
human participants were in accordance with the ethical standards of with and without co-morbid mental retardation. Child Psychiatry
the institutional and/or national research committee and with the 1964 and Human Development, 33(2), 165–172.
Helsinki declaration and its later amendments or comparable ethical Brown, L. (2011). Identity-first language/autistic self advocacy net-
standards. Informed consent was obtained from all individual partici- work. Retrieved May 26, 2017, from http://autisticadvocacy.org/
pants included in the study. about-asan/identity-first-language/.
Carter, A. S., Black, D. O., Tewani, S., Connolly, C. E., Kadlec, M.
B., & Tager-Flusberg, H. (2007). Sex differences in toddlers
with autism spectrum disorders. Journal of Autism and Devel-
References opmental Disorders, 37(1), 86–97. https://doi.org/10.1007/
s10803-006-0331-7.
American Psychiatric Association. (2000). Diagnostic and statistical Chawarska, K., Paul, R., Klin, A., Hannigen, S., Dichtel, L. E., & Volk-
manual of mental disorders (4th ed., text revision). Washington, mar, F. (2007). Parental recognition of developmental problems in
DC: American Psychiatric Association. toddlers with autism spectrum disorders. Journal of Autism and
American Psychiatric Association. (2013). Diagnostic and statistical Developmental Disorders, 37(1), 62–72. https://doi.org/10.1007/
manual of mental disorders (5th ed.). Arlington, VA: American s10803-006-0330-8.
Psychiatric Publishing. Cohen, J. (1988). Statistical power and analysis for the behavioral
Andersson, G. W., Gillberg, C., & Miniscalco, C. (2013). Pre-school sciences (2nd ed.). Hillsdale: Lawrence Erlbaum Associates, Inc.
children with suspected autism spectrum disorders: Do girls and Constantino, J. N., & Gruber, C. (2012). The Social Responsiveness
boys have the same profiles? Research in Developmental Disabili- Scale Manual, Second Edition (SRS-2). Los Angeles: Western
ties, 34(1), 413–422. https://doi.org/10.1016/j.ridd.2012.08.025. Psychological Services.
Auyeung, B., Baron-Cohen, S., Ashwin, E., Knickmeyer, R., Taylor, Constantino, J. N., & Gruber, C. P. (2005). Social responsiveness scale
K., & Hackett, G. (2009). Fetal testosterone and autistic traits. (SRS). Los Angeles: Western Psychological Services.
British Journal of Psychology, 100(1), 1–22. https://doi.org/10.1 Cridland, E. K., Jones, S. C., Caputi, P., & Magee, C. A. (2014). Being
348/000712608X311731. a girl in a boys’ world: Investigating the experiences of girls with
Banach, R., Thompson, A., Szatmari, P., Goldberg, J., Tuff, L., autism spectrum disorders during adolescence. Journal of Autism
Zwaigenbaum, L., & Mahoney, W. (2009). Brief report: Rela- and Developmental Disorders, 44(6), 1261–1274. https://doi.
tionship between non-verbal IQ and Gender in Autism. Journal org/10.1007/s10803-013-1985-6.
of Autism and Developmental Disorders, 39(1), 188–193. https:// Daniels, A. M., & Mandell, D. S. (2014). Explaining differences in age
doi.org/10.1007/s10803-008-0612-4. at autism spectrum disorder diagnosis: A critical review. Autism:
Bargiela, S., Steward, R., & Mandy, W. (2016). The experiences of The International Journal of Research and Practice, 18(5), 583–
late-diagnosed women with autism spectrum conditions: An 597. https://doi.org/10.1177/1362361313480277.
investigation of the female autism phenotype. Journal of Autism Dworzynski, K., Ronald, A., Bolton, P., & Happé, F. (2012). How dif-
and Developmental Disorders, 46(10), 3281–3294. https://doi. ferent are girls and boys above and below the diagnostic threshold
org/10.1007/s10803-016-2872-8. for autism spectrum disorders? Journal of the American Academy
Beatty, P. C., & Willis, G. B. (2007). Research synthesis: The prac- of Child & Adolescent Psychiatry, 51(8), 788–797.
tice of cognitive interviewing. Public Opinion Quarterly, 71(2), Elliot, C. D. (2007). Differential Ability Scales–Second Edition (DAS-
287–311. https://doi.org/10.1093/poq/nfm006. II). San Antonio, TX: Harcourt Assessment.
Begeer, S., Mandell, D., Wijnker-Holmes, B., Venderbosch, S., Farley, M. A., McMahon, W. M., Fombonne, E., Jenson, W. R., Miller,
Rem, D., Stekelenburg, F., & Koot, H. M. (2013). Sex differ- J., Gardner, M., … Coon, H. (2009). Twenty-year outcome for
ences in the timing of identification among children and adults individuals with autism and average or near-average cognitive
with autism spectrum disorders. Journal of Autism and Devel- abilities. Autism Research, 2(2), 109–118. https://doi.org/10.1002/
opmental Disorders, 43(5), 1151–1156. https://doi.org/10.1007/ aur.69.
s10803-012-1656-z. Fombonne, E. (2009). Epidemiology of pervasive developmental dis-
Bejerot, S., Eriksson, J. M., Bonde, S., Carlström, K., Humble, M. B., orders. Pediatric Research, 65(6), 591–598.
& Eriksson, E. (2012). The extreme male brain revisited: Gender Frazier, T. W., Georgiades, S., Bishop, S. L., & Hardan, A. Y. (2014a).
coherence in adults with autism spectrum disorder. The British Behavioral and cognitive characteristics of females and males
Journal of Psychiatry: The Journal of Mental Science, 201, 116– with autism in the simons simplex collection. Journal of the
123. https://doi.org/10.1192/bjp.bp.111.097899. American Academy of Child & Adolescent Psychiatry, 53(3),
329–340. https://doi.org/10.1016/j.jaac.2013.12.004.

13
1710 Journal of Autism and Developmental Disorders (2018) 48:1698–1711

Frazier, T. W., Ratliff, K. R., Gruber, C., Zhang, Y., Law, P. A., & Knickmeyer, R. C., & Baron-Cohen, S. (2006). Fetal testosterone and
Constantino, J. N. (2014b). Confirmatory factor analytic structure sex differences in typical social development and in autism. Jour-
and measurement invariance of quantitative autistic traits meas- nal of Child Neurology, 21(10), 825–845. https://doi.org/10.1177
ured by the social responsiveness scale-2. Autism: The Interna- /08830738060210101601.
tional Journal of Research and Practice, 18(1), 31–44. https://doi. Knickmeyer, R. C., Wheelwright, S., & Baron-Cohen, S. B. (2008).
org/10.1177/1362361313500382. Sex-typical play: Masculinization/defeminization in girls with
Giarelli, E., Wiggins, L. D., Rice, C. E., Levy, S. E., Kirby, R. S., an autism spectrum condition. Journal of Autism and Develop-
Pinto-Martin, J., & Mandell, D. (2010). Sex differences in the mental Disorders, 38(6), 1028–1035. https://doi.org/10.1007/
evaluation and diagnosis of autism spectrum disorders among s10803-007-0475-0.
children. Disability and Health Journal, 3(2), 107–116. https:// Kreiser, N., & White, S. (2014). ASD in females: Are we overstating
doi.org/10.1016/j.dhjo.2009.07.001. the gender difference in diagnosis? Clinical Child and Family Psy-
Gilman, S. R., Iossifov, I., Levy, D., Ronemus, M., Wigler, M., & chology Review. Retrieved from http://link.springer.com/article/
Vitkup, D. (2011). Rare de novo variants associated with autism https://doi.org/10.1007/s10567-013-0148-9.
implicate a large functional network of genes involved in forma- Lai, M.-C., Baron-Cohen, S., & Buxbaum, J. D. (2015). Understanding
tion and function of synapses. Neuron, 70(5), 898–907. https:// autism in the light of sex/gender. Molecular Autism, 6(1). https://
doi.org/10.1016/j.neuron.2011.05.021. doi.org/10.1186/s13229-015-0021-4.
Halladay, A. K., Bishop, S., Constantino, J. N., Daniels, A. M., Koenig, Lai, M.-C., Lombardo, M. V., Ruigrok, A. N., Chakrabarti, B., Auye-
K., Palmer, K., … Szatmari, P. (2015). Sex and gender differences ung, B., Szatmari, P. … MRC AIMS Consortium. (2016). Quanti-
in autism spectrum disorder: Summarizing evidence gaps and fying and exploring camouflaging in men and women with autism.
identifying emerging areas of priority. Molecular Autism, 6(1), Autism. https://doi.org/10.1177/1362361316671012.
36. https://doi.org/10.1186/s13229-015-0019-y. Little, L. M., Wallisch, A., Salley, B., & Jamison, R. (2016). Do early
Hartley, S. L., & Sikora, D. M. (2009). Sex differences in autism spec- caregiver concerns differ for girls with autism spectrum disorders?
trum disorder: An examination of developmental functioning, Autism. https://doi.org/10.1177/1362361316664188.
autistic symptoms, and coexisting behavior problems in toddlers. Loomes, R., Hull, L., & Mandy, W. P. L. (2017). What is the male-to-
Journal of Autism and Developmental Disorders, 39(12), 1715– female ratio in autism spectrum disorder? A systematic review
1722. https://doi.org/10.1007/s10803-009-0810-8. and meta-analysis. Journal of the American Academy of Child &
Hiller, R. M., Young, R. L., & Weber, N. (2016). Sex differences Adolescent Psychiatry. https://doi.org/10.1016/j.jaac.2017.03.013.
in pre-diagnosis concerns for children later diagnosed with Lord, C., Rutter, M., DiLavore, P., Risi, S., Gotham, K., & Bishop,
autism spectrum disorder. Autism, 20(1), 75–84. https://doi. S. (2012). Autism Diagnostic Observation Schedule–2nd Edition
org/10.1177/1362361314568899. (ADOS-2). Los Angeles: Western Psychological Corporation.
Holtmann, M., Bölte, S., & Poustka, F. (2007). Autism spec- Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. S. (2001). Autism
trum disorders: Sex differences in autistic behaviour Diagnostic Observation Schedule: Manual. Los Angeles: Western
domains and coexisting psychopathology. Developmental Psychological Services.
Medicine & Child Neurology, 49(5), 361–366. https://doi. Lord, C., & Schopler, E. (1985). Brief report: Differences in sex ratios
org/10.1111/j.1469-8749.2007.00361.x. in autism as a function of measured intelligence. Journal of
Howe, Y. J., O’Rourke, J. A., Yatchmink, Y., Viscidi, E. W., Jones, R. Autism and Developmental Disorders, 15(2), 185–193. https://
N., & Morrow, E. M. (2015). Female autism phenotypes investi- doi.org/10.1007/BF01531604.
gated at different levels of language and developmental abilities. Lord, C., Schopler, E., & Revicki, D. (1982). Sex differences in autism.
Journal of Autism and Developmental Disorders, 45(11), 3537– Journal of Autism and Developmental Disorders, 12(4), 317–330.
3549. https://doi.org/10.1007/s10803-015-2501-y. https://doi.org/10.1007/BF01538320.
Jacquemont, S., Coe, B. P., Hersch, M., Duyzend, M. H., Krumm, Mandic-Maravic, V., Pejovic-Milovancevic, M., Mitkovic-Voncina,
N., Bergmann, S., … Eichler, E. E. (2014). A higher mutational M., Kostic, M., Aleksic-Hil, O., Radosavljev-Kircanski, J., …
burden in females supports a “female protective model” in neu- Lecic-Tosevski, D. (2015). Sex differences in autism spectrum
rodevelopmental disorders. American Journal of Human Genetics, disorders: Does sex moderate the pathway from clinical symp-
94(3), 415–425. https://doi.org/10.1016/j.ajhg.2014.02.001. toms to adaptive behavior? Scientific Reports, 5, 10418. https://
Kanne, S. M., Gerber, A. J., Quirmbach, L. M., Sparrow, S. S., Cic- doi.org/10.1038/srep10418.
chetti, D. V., & Saulnier, C. A. (2011). The role of adaptive behav- Mandy, W., Chilvers, R., Chowdhury, U., Salter, G., Seigal, A., &
ior in autism spectrum disorders: Implications for functional out- Skuse, D. (2012). Sex differences in autism spectrum disorder:
come. Journal of Autism and Developmental Disorders, 41(8), Evidence from a large sample of children and adolescents. Jour-
1007–1018. https://doi.org/10.1007/s10803-010-1126-4. nal of Autism and Developmental Disorders, 42(7), 1304–1313.
Kataoka, S., Takuma, K., Hara, Y., Maeda, Y., Ago, Y., & Matsuda, https://doi.org/10.1007/s10803-011-1356-0.
T. (2013). Autism-like behaviours with transient histone hypera- McLennan, J. D., Lord, C., & Schopler, E. (1993). Sex differences
cetylation in mice treated prenatally with valproic acid. The Inter- in higher functioning people with autism. Journal of Autism
national Journal of Neuropsychopharmacology, 16(1), 91–103. and Developmental Disorders, 23(2), 217–227. https://doi.
https://doi.org/10.1017/S1461145711001714. org/10.1007/BF01046216.
Kirkovski, M., Enticott, P. G., & Fitzgerald, P. B. (2013). A review of Messinger, D. S., Young, G. S., Webb, S. J., Ozonoff, S., Bryson, S.
the role of female gender in autism spectrum disorders. Journal of E., Carter, A., … Zwaigenbaum, L. (2015). Early sex differences
Autism and Developmental Disorders, 43(11), 2584–2603. https:// are not autism-specific: A Baby Siblings Research Consortium
doi.org/10.1007/s10803-013-1811-1. (BSRC) study. Molecular Autism, 6(1). https://doi.org/10.1186/
Klin, A., Saulnier, C. A., Sparrow, S. S., Cicchetti, D. V., Volkmar, s13229-015-0027-y.
F. R., & Lord, C. (2007). Social and communication abilities Øien, R. A., Hart, L., Schjølberg, S., Wall, C. A., Kim, E. S., Nordahl-
and disabilities in higher functioning individuals with autism Hansen, A., … Shic, F. (2017). Parent-endorsed sex differences in
spectrum disorders: The Vineland and the ADOS. Journal of toddlers with and without ASD: Utilizing the M-CHAT. Journal
Autism and Developmental Disorders, 37(4), 748–759. https:// of Autism and Developmental Disorders, 47(1), 126–134. https://
doi.org/10.1007/s10803-006-0229-4. doi.org/10.1007/s10803-016-2945-8.

13
Journal of Autism and Developmental Disorders (2018) 48:1698–1711 1711

Pilowsky, T., Yirmiya, N., Shulman, C., & Dover, R. (1998). The Trubanova, A., Donlon, K., Kreiser, N. L., Ollendick, T. H., & White,
autism diagnostic interview-revised and the childhood autism S. W. (2014). Under-identification of ASD in females: A case
rating scale: Differences Between diagnostic systems and series illustrating the unique presentation of ASD in young adult
comparison between genders. Journal of Autism and Devel- females. Scandinavian Journal of Child and Adolescent Psychia-
opmental Disorders, 28(2), 143–151. https://doi.org/10.102 try and Psychology, 2(2), 66–76.
3/A:1026092632466. Tsai, L. Y., & Beisler, J. M. (1983). The development of sex differences
Pine, D. S., Guyer, A. E., Goldwin, M., Towbin, K. A., & Leibenluft, in infantile autism. The British Journal of Psychiatry, 142(4),
E. (2008). Autism spectrum disorder scale scores in pediatric 373–378. https://doi.org/10.1192/bjp.142.4.373.
mood and anxiety disorders. Journal of the American Academy Van Wijngaarden-Cremers, P. J. M., van Eeten, E., Groen, W. B., Van
of Child and Adolescent Psychiatry, 47(6), 652–661. https://doi. Deurzen, P. A., Oosterling, I. J., & Van der Gaag, R. J. (2014).
org/10.1097/CHI.0b013e31816bffa5. Gender and age differences in the core triad of impairments in
Pugliese, C. E., Anthony, L., Strang, J. F., Dudley, K., Wallace, G. autism spectrum disorders: A systematic review and meta-anal-
L., & Kenworthy, L. (2015). Increasing adaptive behavior skill ysis. Journal of Autism and Developmental Disorders, 44(3),
deficits from childhood to adolescence in autism spectrum dis- 627–635. https://doi.org/10.1007/s10803-013-1913-9.
order: Role of executive function. Journal of Autism and Devel- Volkmar, F., Sparrow, S. S., Goudreau, D., Cicchetti, D. V., Paul, R.,
opmental Disorders, 45, 1579–1587. https://doi.org/10.1007/ & Cohen, D. J. (1987). Social deficits in autism: An operational
s10803-014-2309-1. approach using the Vineland Adaptive Behavior Scales. Journal of
Reinhardt, V. P., Wetherby, A. M., Schatschneider, C., & Lord, C. the American Academy of Child & Adolescent Psychiatry, 26(2),
(2015). Examination of sex differences in a large sample of young 156–161. https://doi.org/10.1097/00004583-198703000-00005.
children with autism spectrum disorder and typical development. Volkmar, F. R., Szatmari, P., & Sparrow, S. S. (1993). Sex differ-
Journal of Autism and Developmental Disorders, 45(3), 697–706. ences in pervasive developmental disorders. Journal of Autism
https://doi.org/10.1007/s10803-014-2223-6. and Developmental Disorders, 23(4), 579–591. https://doi.
Robinson, E. B., Lichtenstein, P., Anckarsater, H., Happé, F., & Ron- org/10.1007/BF01046103.
ald, A. (2013). Examining and interpreting the female protective Wechsler, D. (2003). Wechsler Intelligence Scale for Children–
effect against autistic behavior. Proceedings of the National Acad- Fourth Edition (WISC-IV). San Antonio, TX: The Psychological
emy of Sciences, 110(13), 5258–5262. https://doi.org/10.1073/ Corporation.
pnas.1211070110. Wechsler, D. (2008). Wechsler Adult Intelligence Scale-Fourth
Rutter, M., Le Couteur, A., & Lord, C. (2003). Autism diagnostic Edition (WAIS-IV). San Antonio, TX: The Psychological
interview-revised (Vol. 29, p. 30). Los Angeles: Western Psycho- Corporation-Pearson.
logical Services. Wechsler, D. (2011). Wechsler abbreviated scale of intelligence–Sec-
Schoch, H., Kreibich, A. S., Ferri, S. L., White, R. S., Bohorquez, ond edition (WASI-II). San Antonio, TX: NCS Pearson.
D., Banerjee, A., … Brodkin, E. S. (2017). Sociability deficits Wechsler, D. (2014). WPPSI-IV: Wechsler Preschool and Primary
and altered amygdala circuits in mice lacking Pcdh10, an autism Scale of Intelligence-Fourth Edition technical and interpretive
associated gene. Biological Psychiatry, 81(3), 193–202. https:// manual. San Antonio, TX: Pearson.
doi.org/10.1016/j.biopsych.2016.06.008. Wechsler, D. (2014). Wechsler Intelligence Scale for Children–
Shattuck, P. T., Durkin, M., Maenner, M., Newschaffer, C., Mandell, Fifth Edition (WISC-V). Bloomington, MN: The Psychological
D. S., Wiggins, L., … Cuniff, C. (2009). Timing of identification Corporation.
among children with an autism spectrum disorder: Findings from Wechsler, D., & Hsiao-pin, C. (2011). WASI-II: Wechsler abbreviated
a population-based surveillance study. Journal of the American scale of intelligence. Bloomington: Pearson.
Academy of Child & Adolescent Psychiatry, 48(5), 474–483. Wilson, C. E., Murphy, C. M., McAlonan, G., Robertson, D. M., Spain,
https://doi.org/10.1097/CHI.0b013e31819b3848. D., Hayward, H., … Zinkstok, J. (2016). Does sex influence the
Siklos, S., & Kerns, K. A. (2007). Assessing the diagnostic experiences diagnostic evaluation of autism spectrum disorder in adults?
of a small sample of parents of children with autism spectrum Autism, 20:808–819.
disorders. Research in Developmental Disabilities, 28(1), 9–22. Yerys, B. E., Wallace, G. L., Sokoloff, J. L., Shook, D. A., James,
https://doi.org/10.1016/j.ridd.2005.09.003. J. D., & Kenworthy, L. (2009). Attention deficit/hyperactivity
Sparrow, S. S., Balla, D. A., & Cicchetti, D. V. (2005). Vineland-II disorder symptoms moderate cognition and behavior in children
adaptive behavior scales. Circle Pines: AGS Publishing. with autism spectrum disorders. Autism Research: Official Journal
Strang, J. F., Kenworthy, L., Dominska, A., Sokoloff, J., Kenealy, L. of the International Society for Autism Research, 2(6), 322–333.
E., Berl, M., … Wallace, G. L. (2014). Increased gender variance https://doi.org/10.1002/aur.103.
in autism spectrum disorders and attention deficit hyperactivity
disorder. Archives of Sexual Behavior, 43(8), 1525–1533. https://
doi.org/10.1007/s10508-014-0285-3.

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