Journal of Autism and Developmental Disorders

, Volume 45, Issue 11, pp 3537–3549 | Cite as

Female Autism Phenotypes Investigated at Different Levels of Language and Developmental Abilities

  • Yamini J. Howe
  • Julia A. O’Rourke
  • Yvette Yatchmink
  • Emma W. Viscidi
  • Richard N. Jones
  • Eric M. MorrowEmail author
Original Paper


This study investigated the differences in clinical symptoms between females and males with autism spectrum disorder (ASD) across three verbal ability groups (nonverbal, phrase and fluent speech), based on which Autism Diagnostic Observation Schedule module was administered to 5723 individuals in four research datasets. In the Simons Simplex Collection and Autism Treatment Network, females with ASD and phrase or fluent speech had lower cognitive, adaptive, and social abilities than males. In the Autism Genetics Resource Exchange and the Autism Consortium, females with phrase or fluent speech had similar or better adaptive and social abilities than males. Females who were nonverbal had similar cognitive, adaptive, and social abilities as males. Population-based longitudinal studies of verbally fluent females with ASD are needed.


Autism spectrum disorder Sex differences Diagnosis of autism spectrum disorder 



EMM has received support from NIH P20GM103645-01A1, R01MH105442-01, R01MH102418, and a Career Award in Medical Science from the Burroughs Wellcome Fund. YJH received support from the Maternal Child Health Bureau (MCHB) under training Grant T77MC09797. We gratefully acknowledge the resources provided by the Autism Genetic Resource Exchange (AGRE) Consortium and the participating AGRE families. The AGRE is a program of Autism Speaks and is supported, in part, by Grant 1U24MH081810 from the National Institute of Mental Health to Clara M. Lajonchere (PI). We would also like to acknowledge datasets used for the analyses obtained from the Autism Treatment Network (ATN) Database. Funding support for ATN was provided by Autism Speaks. We would like to thank the ATN participants and the ATN Research Group for their valuable contribution to this research. The Autism Consortium is a Boston-based clinical and research collaboration, with 17 institutional members and 125 individual scientist and clinician members, who are collectively dedicated to catalyzing progress in understanding autism and related neurodevelopmental disorders in order to improve diagnosis, clinical care and treatment. With data and samples collected from 525+ families who participated in clinical research, the Consortium’s repository is made available for use by the autism research community. The authors are grateful to the Consortium, its members and the families who have made this vital resource possible. We are also grateful to all of the families at the participating SSC Simplex Collection (SSC) sites, as well as the principal investigators (A. Beaudet, R. Bernier, J. Constantino, E. Cook, E. Fombonne, D. Geschwind, D. Grice, A. Klin, D. Ledbetter, C. Lord, C. Martin, D. Martin, R. Maxim, J. Miles, O. Ousley, B. Peterson, J. Piggot, C. Saulnier, M. State, W. Stone, J. Sutcliffe, C. Walsh, E. Wijsman).


  1. Achenbach, T. M., & Rescorla, L. (2001). Manual for the ASEBA school-age forms & profiles: An integrated system of multi-informant assessment. Burlington, VT: ASEBA.Google Scholar
  2. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Publishing.Google Scholar
  3. Autism and Developmental Disabilities Monitoring (ADDM) Network Surveillance Year 2010 Principal Investigators; CDC. (2014). Prevalence of autism spectrum disorder among children aged 8 years—autism and developmental disabilities monitoring network, 11 sites, United States, 2010. MMWR Surveillance Summaries, 63(2), 1–21.Google Scholar
  4. Banach, R., Thompson, A., Szatmari, P., Goldberg, J., Tuff, L., Zwaigenbaum, L., & Mahoney, W. (2009). Brief Report: relationship between non-verbal IQ and gender in autism. Journal of Autism and Developmental Disorders, 39(1), 188–193.CrossRefPubMedGoogle Scholar
  5. Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B, 57, 289–300.Google Scholar
  6. Bolte, S., Dziobek, I., & Poustka, F. (2009). Brief report: The level and nature of autistic intelligence revisited. [Comparative Study]. Journal of Autism and Developmental Disorders, 39(4), 678–682.CrossRefPubMedGoogle Scholar
  7. Cohen, J. (1987). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Erlbaum.Google Scholar
  8. Constantino, J. N., Davis, S. A., Todd, R. D., Schindler, M. K., Gross, M. M., Brophy, S. L., & Reich, W. (2003). Validation of a brief quantitative measure of autistic traits: Comparison of the social responsiveness scale with the autism diagnostic interview-revised. Journal of Autism and Developmental Disorders, 33(4), 427–433.CrossRefPubMedGoogle Scholar
  9. Constantino, J. N., & Todd, R. D. (2003). Autistic traits in the general population: A twin study. Archives of General Psychiatry, 60(5), 524–530.CrossRefPubMedGoogle Scholar
  10. Cook, E. H, Jr, & Scherer, S. W. (2008). Copy-number variations associated with neuropsychiatric conditions. Nature, 455(7215), 919–923.CrossRefPubMedGoogle Scholar
  11. Coury, D., Jones, N., Klatka, K., Winklosky, B., & Perrin, J. (2009). Healthcare for children with autism: The Autism Treatment Network. Current Opinion in Pediatrics, 21(6), 828–832.CrossRefPubMedGoogle Scholar
  12. de Bildt, A., Sytema, S., Ketelaars, C., Kraijer, D., Mulder, E., Volkmar, F., & Minderaa, R. (2004). Interrelationship between autism diagnostic observation schedule-generic (ADOS-G), autism diagnostic interview-revised (ADI-R), and the diagnostic and statistical manual of mental disorders (DSM-IV-TR) classification in children and adolescents with mental retardation. Journal of Autism and Developmental Disorders, 34(2), 129–137.CrossRefPubMedGoogle Scholar
  13. Dworzynski, K., Ronald, A., Bolton, P., & Happe, F. (2012). How different are girls and boys above and below the diagnostic threshold for autism spectrum disorders? Journal of the American Academy of Child and Adolescent Psychiatry, 51(8), 788–797.CrossRefPubMedGoogle Scholar
  14. Ehlers, S., Gillberg, C., & Wing, L. (1999). A screening questionnaire for Asperger syndrome and other high-functioning autism spectrum disorders in school age children. Journal of Autism and Developmental Disorders, 29(2), 129–141.CrossRefPubMedGoogle Scholar
  15. Elliott, C. D. (1990). Differential ability scales: Introductory and technical handbook. San Antonio: Psychological Corp., Harcourt Brace Jovanovich.Google Scholar
  16. Elliott, A. C., & Reisch, J. S. (2003). Implementing a multiple comparison test for proportions in a 2xC crosstabulation in SAS®. In Proceedings of the thirty first annual SAS user group international conference, 20431. Cary, NC: SAS Institute Inc.Google Scholar
  17. Fischbach, G. D., & Lord, C. (2010). The Simons Simplex Collection: A resource for identification of autism genetic risk factors. Neuron, 68(2), 192–195.CrossRefPubMedGoogle Scholar
  18. Fombonne, E. (2003). Epidemiological surveys of autism and other pervasive developmental disorders: An update. Journal of Autism and Developmental Disorders, 33(4), 365–382.CrossRefPubMedGoogle Scholar
  19. Frazier, T. W., Georgiades, S., Bishop, S. L., & Hardan, A. Y. (2014). Behavioral and cognitive characteristics of females and males with autism in the Simons Simplex Collection. Journal of the American Academy of Child and Adolescent Psychiatry, 53(3), 329–340.PubMedCentralCrossRefPubMedGoogle Scholar
  20. Goldman, S. (2013). Opinion: Sex, gender and the diagnosis of autism—a biosocial view of the male preponderance. Research in Autism Spectrum Disorders, 7(6), 675–679.PubMedCentralCrossRefPubMedGoogle Scholar
  21. Gotham, K., Risi, S., Pickles, A., & Lord, C. (2007). The autism diagnostic observation schedule: Revised algorithms for improved diagnostic validity. Journal of Autism and Developmental Disorders, 37(4), 613–627.CrossRefPubMedGoogle Scholar
  22. Holtmann, M., Bolte, S., & Poustka, F. (2007). Autism spectrum disorders: Sex differences in autistic behaviour domains and coexisting psychopathology. Developmental Medicine and Child Neurology, 49(5), 361–366.CrossRefPubMedGoogle Scholar
  23. Jensen, C. M., Steinhausen, H. C., & Lauritsen, M. B. (2014). Time trends over 16 years in incidence-rates of autism spectrum disorders across the lifespan based on nationwide Danish register data. Journal of Autism and Developmental Disorders, 44(8), 1808–1818.CrossRefPubMedGoogle Scholar
  24. Kim, Y. S., Leventhal, B. L., Koh, Y. J., Fombonne, E., Laska, E., Lim, E. C., & Grinker, R. R. (2011). Prevalence of autism spectrum disorders in a total population sample. American Journal of Psychiatry, 168(9), 904–912.CrossRefPubMedGoogle Scholar
  25. Konstantareas, M. M., Homatidis, S., & Busch, J. (1989). Cognitive, communication, and social differences between autistic boys and girls. Journal of Applied Developmental Psychology, 10(4), 411–424.CrossRefGoogle Scholar
  26. Kraemer, H. C., Morgan, G. A., Leech, N. L., Gliner, J. A., Vaske, J. J., & Harmon, R. J. (2003). Measures of clinical significance. Journal of the American Academy of Child and Adolescent Psychiatry, 42(12), 1524–1529.CrossRefPubMedGoogle Scholar
  27. Lai, M. C., Lombardo, M. V., Auyeung, B., Chakrabarti, B., & Baron-Cohen, S. (2015). Sex/gender differences and autism: setting the scene for future research. Journal of the American Academy of Child and Adolescent Psychiatry, 54(1), 11–24.PubMedCentralCrossRefPubMedGoogle Scholar
  28. Lai, M. C., Lombardo, M. V., Pasco, G., Ruigrok, A. N., Wheelwright, S. J., Sadek, S. A., & Baron-Cohen, S. (2011). A behavioral comparison of male and female adults with high functioning autism spectrum conditions. Public Library of Science One, 6(6), e20835.PubMedCentralPubMedGoogle Scholar
  29. Lajonchere, C. M. (2010). Changing the landscape of autism research: The autism genetic resource exchange. Neuron, 68(2), 187–191.PubMedCentralCrossRefPubMedGoogle Scholar
  30. Lajonchere, C., Jones, N., Coury, D., & Perrin, J. (2012). Leadership in health care, research and quality improvement for children and adolescents with autism spectrum disorders: Autism Treatment Network and autism intervention research network on physical healthy. Pediatrics, 130(Supplement 2), S62–S68.CrossRefPubMedGoogle Scholar
  31. Lord, C., DiLavore, P. C., & Risi, S. (2002). Autism diagnostic observation schedule. Los Angeles, CA: Western Psychological Services.Google Scholar
  32. Lord, C., Risi, S., Lambrecht, L., Cook, E. H, Jr, Leventhal, B. L., DiLavore, P. C., & Rutter, M. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223.CrossRefPubMedGoogle Scholar
  33. Lord, C., Rutter, M., Goode, S., Heemsbergen, J., Jordan, H., Mawhood, L., & Schopler, E. (1989). Autism diagnostic observation schedule: a standardized observation of communicative and social behavior. Journal of Autism and Developmental Disorders, 19(2), 185–212.CrossRefPubMedGoogle Scholar
  34. Lord, C., Schopler, E., & Revicki, D. (1982). Sex differences in autism. Journal of Autism and Developmental Disorders, 12(4), 317–330.CrossRefPubMedGoogle Scholar
  35. Mandy, W., Chilvers, R., Chowdhury, U., Salter, G., Seigal, A., & Skuse, D. (2012). Sex differences in autism spectrum disorder: Evidence from a large sample of children and adolescents. Journal of Autism and Developmental Disorders, 42(7), 1304–1313.CrossRefPubMedGoogle Scholar
  36. Mattila, M. L., Kielinen, M., Linna, S. L., Jussila, K., Ebeling, H., Bloigu, R., & Moilanen, I. (2011). Autism spectrum disorders according to DSM-IV-TR and comparison with DSM-5 draft criteria: An epidemiological study. Journal of the American Academy of Child and Adolescent Psychiatry, 50(6), 583–592.CrossRefPubMedGoogle Scholar
  37. Mottron, L. (2004). Matching strategies in cognitive research with individuals with high-functioning autism: Current practices, instrument biases, and recommendations. Journal of Autism and Developmental Disorders, 34(1), 19–27.CrossRefPubMedGoogle Scholar
  38. Robinson, E. B., Lichtenstein, P., Anckarsäter, H., Happé, F., & Ronald, A. (2013). Examining and interpreting the female protective effect against autistic behavior. Proceedings of the National Academy of Sciences U S A, 110(13), 5258–5262.CrossRefGoogle Scholar
  39. Roid, G. H. (2003). Stanford-binet intelligence scales (5th ed.). Itasca, IL: Riverside.Google Scholar
  40. Rutter, M., Le Couteur, A., & Lord, C. (2003). Autism diagnostic interview-Revised. Los Angeles, CA: Western Psychological Services.Google Scholar
  41. Scott, F. J., Baron-Cohen, S., Bolton, P., & Brayne, C. (2002). Brief report: Prevalence of autism spectrum conditions in children aged 5–11 years in Cambridgeshire, UK. Autism, 6(3), 231–237.CrossRefPubMedGoogle Scholar
  42. Shen, Y., Dies, K. A., Holm, I. A., Bridgemohan, C., Sobeih, M. M., Caronna, E. B., & Miller, D. T. (2010). Clinical genetic testing for patients with autism spectrum disorders. Pediatrics, 125(4), e727–e735.PubMedCentralCrossRefPubMedGoogle Scholar
  43. Skuse, D. H., Mandy, W., Steeer, C., Miller, L. L., Goodman, R., Lawrence, K., et al. (2009). Social communication competence and functional adaptation in a general population of children: Preliminary evidence for sex-by-verbal IQ differential risk. Journal of the American Academy of Child and Adolescent Psychiatry, 48(2), 128–137.CrossRefPubMedGoogle Scholar
  44. Solomon, M., Miller, M., Taylor, S. L., Hinshaw, S. P., & Carter, C. S. (2012). Autism symptoms and internalizing psychopathology in girls and boys with autism spectrum disorders. Journal of Autism and Developmental Disorders, 42(1), 48–59.PubMedCentralCrossRefPubMedGoogle Scholar
  45. Sparrow, S. S., Cicchetti, D. V., & Balla, D. A. (2005). Vineland adaptive behavior scales, second edition (Vineland-II). San Antonio, TX: Psychological Corp.Google Scholar
  46. Volkmar, F. R., Szatmari, P., & Sparrow, S. S. (1993). Sex differences in pervasive developmental disorders. Journal of Autism and Developmental Disorders, 23(4), 579–591.CrossRefPubMedGoogle Scholar
  47. Wechsler, D. (1999). Wechsler abbreviated scales of intelligence (WASI). San Antonio, TX: Psychological Corp.Google Scholar
  48. Wechsler, D. (2002). Wechsler primary and preschool scale of intelligence-third edition (WPPSI-III). San Antonio, TX: Harcourt Assessment.Google Scholar
  49. Wechsler, D. (2004). Wechsler intelligence scale for children-fourth edition (WISC-IV). London, UK: Pearson Assessment.Google Scholar
  50. Yeargin-Allsopp, M., Rice, C., Karapurkar, T., Doernberg, N., Boyle, C., & Murphy, C. (2003). Prevalence of autism in a US metropolitan area. JAMA, 289(1), 49–55.CrossRefPubMedGoogle Scholar
  51. Zwaigenbaum, L., Bryson, S. E., Szatmari, P., Brian, J., Smith, I. M., Roberts, W., et al. (2012). Sex differences in children with autism spectrum disorder identified within a high-risk infant cohort. Journal of Autism and Developmental Disorders, 42(12), 2585–2596.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Yamini J. Howe
    • 1
    • 8
  • Julia A. O’Rourke
    • 2
    • 3
  • Yvette Yatchmink
    • 1
  • Emma W. Viscidi
    • 4
    • 9
  • Richard N. Jones
    • 5
  • Eric M. Morrow
    • 5
    • 6
    • 7
    Email author
  1. 1.Division of Developmental Behavioral Pediatrics, Department of Pediatrics, Hasbro Children’s/Rhode Island HospitalBrown UniversityProvidenceUSA
  2. 2.Lurie Center for AutismMassachusetts General Hospital for ChildrenLexingtonUSA
  3. 3.Laboratory of Computer ScienceMassachusetts General HospitalBostonUSA
  4. 4.Division of Biology and Medicine, Department of Community Health/EpidemiologyBrown UniversityProvidenceUSA
  5. 5.Department of Psychiatry and Human BehaviorBrown University Medical SchoolProvidenceUSA
  6. 6.Department of Molecular Biology, Cell Biology and Biochemistry and Institute for Brain ScienceBrown UniversityProvidenceUSA
  7. 7.Developmental Disorders Genetics Research ProgramEmma Pendleton Bradley HospitalProvidenceUSA
  8. 8.Lurie Center for AutismMassachusetts General Hospital for ChildrenLexingtonUSA
  9. 9.BiogenCambridgeUSA

Personalised recommendations