Sign In

Login to our social questions & Answers Engine to ask questions answer people’s questions & connect with other people.

Forgot Password

Lost your password? Please enter your email address. You will receive a link and will create a new password via email.

You must login to ask question.

Please briefly explain why you feel this question should be reported.

Please briefly explain why you feel this answer should be reported.

Please briefly explain why you feel this user should be reported.

Read an article

Please view explanation and answer below.


Sex differences in the protection of host
immune systems by a polyembryonic
Hideki Nishikawa1,†, Jin Yoshimura2,3,4 and Kikuo Iwabuchi1



Faculty of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo 183-8509, Japan
Graduate School of Science and Technology, Shizuoka University, Hamamatsu, 432-8561, Japan
Department of Environmental and Forest Biology, SUNY-CESF, Syracuse, NY 13210, USA
Marine Biosystems Research Center, Chiba University, Kamogawa, Chiba 299-5502, Japan

Downloaded from on 21 September 2022


Cite this article: Nishikawa H, Yoshimura J,
Iwabuchi K. 2013 Sex differences in the
protection of host immune systems by a
polyembryonic parasitoid. Biol Lett 9:

Received: 27 September 2013
Accepted: 29 November 2013

Subject Areas:
cellular biology, ecology, evolution,
developmental biology
Copidosoma floridanum, multi-parasitism,
haemocyte counts, immune response,
Glyptapanteles pallipes

Author for correspondence:
Jin Yoshimura

Present address: Department of Integrated
Biosciences, Graduate School of Frontier
Sciences, University of Tokyo, Kashiwa,
Chiba 277-8562, Japan.
Electronic supplementary material is available
at or

Endoparasitoids have the ability to evade the cellular immune responses of a
host and to create an environment suitable for survival of their progeny
within a host. Generally, the host immune system is suppressed by endoparasitoids. However, polyembryonic endoparasitoids appear to invade their hosts
using molecular mimicry rather than immune system suppression. It is not
known how the host immune system is modified by polyembryonic endoparasitoids. Using haemocyte counts and measurement of cellular immune
responses, we evaluated modification of the host immune system after separate
infestations by a polyembryonic parasitoid (Copidosoma floridanum) and another
parasitoid (Glyptapanteles pallipes) and by both together (multi-parasitism). We
found that the polyembryonic parasitoid maintains and enhances the host
immune system, whereas the other parasitoid strongly suppresses the immune
system. Multi-parasitization analysis revealed that C. floridanum cancelled the
immune suppression by G. pallipes and strengthened the host immunity. This
enhancement was much stronger with male than with female C. floridanum.

1. Introduction
Endoparasitoids develop in a host haemocoel by consuming haemolymph and
later the internal organs, and eventually kill the host [1]. Various physiological
interactions and regulations exist between the parasitoid and the host. The most
important challenge for parasitoids is to circumvent the host cellular immune
response, which will lead to haemocytic encapsulation [2,3]. Many parasitoids
are known to suppress host immunity [4]; for example, some parasitoids in the
Braconidae and Ichneumonidae suppress it by maternal secretions of polydnaviruses, venom and ovarian proteins [2,5,6]. However, such suppression is
likely to enhance the host’s susceptibility to fungal, bacterial and viral infections
[7], resulting in an immunological dilemma for the parasitoids.
The polyembryonic parasitoid Copidosoma floridanum appears to have solved
this dilemma in a unique way. This species exhibits clonal reproduction in
which one egg yields several thousand reproductive larvae and about a hundred soldier larvae, all of which evade the host’s immune responses by
molecular mimicry [8–10]. Both the embryo and larva of this species are surrounded by an extraembryonic syncytium (membrane) that shields these life
stages from the host cellular immune response [11], thereby circumventing
the need for immunological suppression of the parasitized host.
Another important observation on host immunity comes from studies of
multi-parasitism [1]. When a single host is parasitized by two different parasitoids, one parasitoid species emerges victorious following competition between
them. Previous studies have shown that C. floridanum usually kills and eliminates the larvae of its competitor, Glyptapanteles pallipes (Braconidae) by attacking
them with soldier larvae and a unique toxic humoral factor [12]. There are

& 2013 The Author(s) Published by the Royal Society. All rights reserved.

Table 1. Percent DHCs for C. agnata parasitized by C. floridanum (male or female), G. pallipes alone, and multi-parasitized by C. floridanum and G. pallipes.
Cf, C. floridanum; Gp, G. pallipes.








31.3 + 4.9a

39.7 + 5.9ab

12.4 + 3.7a

13.9 + 5.0a

2.7 + 1.6a

parasitized by:
CfF alone


38.6 + 4.9ab

35.9 + 3.6a

12.2 + 2.6a

11.9 + 4.4ab…


Leave a comment