Speaker for the Dead begins 3000 years after the events of Ender's Game. Ender is departing the planet where his sister Valentine has found a husband. He has also acquired an integrated computer by which he communicates with a powerful artificial intelligence known as Jane. Her existence is known only to Ender. He has taken the role of a Speaker for the Dead, keeping his identity as the "Ender the Xenocide", who orchestrated the victory over the Formics, a secret. His book, "The Hive Queen and the Hegemon", in which he "spoke" for the dead Formics, was a self-critical work that was intended to portay Ender as a heartless monster who destroyed a sentient race. The name "Ender" is now considered a vile insult.
Ender departs for the planet Lusitania, where a request has been made to "speak" on behalf of a researcher who has died from contact with the planet's indigenous species, the piggies. When he arrives at the planet 22 years later (relativity having aged him only slightly; less than two weeks) he finds that the original call for a Speaker has been rescinded. Two other requests, however, have been made to "speak" for more recent deaths. Ender discovers that both calls originated from the same family; the first from Novinha's daughter Ela requesting someone speak for the death of Novinha's husband Marcos, and the second from her eldest son Miro, who has asked for a speaker for the researcher Libo.
Ender begins to investigate the Marcos figure and has frequent contact with Novinha's family. His honest and open approach endears him to most of the children as a father figure. He discovers that Marcos was abusive to his wife and children. With the help of Jane and his connection with the children, he uncovers multiple secrets that have been hidden for years. However, while in dialogue with the Children of the Mind, the planet's religious monastic order, he is annoyed by Jane's semi-sarcastic commentary and turns off his connection to her, something he has never done before. The resulting complete isolation and trauma of Jane is the unforeseen result. Jane, without consulting Ender, sends incriminating reports to the intersteller authorities who order the arrest of Miro and Ouanda, the researchers and lovers who have been investigating the piggies. The colony's charter is cancelled and the colonist are forced to rely on Ender for guidance.
Meanwhile, Ender has been receiving pressure from the Hive-Queen's pupa to allow her to settle on this world because she has been in telepathic contact with another race. Ender assumes this race is the piggies, although the bipedal life forms that are the primary contacts of Miro and Ouanda seem very simple and not telepathic at all. After the sanctions are put in place, he gets Miro and Ouanda to allow him to visit the piggies, who have been asking to meet him, the 'original Speaker' (a claim Miro and Ouanda have been dismissing as a misunderstanding). Ender reverts many of the researchers assumptions when he not only admits to being the original Speaker, but has the piggies demonstrate that the trees the piggies grow from the corpses of those who have been ritually killed is the third, reproductive stage. The ritual killings of the two xenologers were misunderstandings. The piggies were under the false impression that humans reproduced in a fashion similar to themselves.
After these revelations, Ender proceeds to "speak" for Marcos and revealed many secrets hitherto hidden, mostly by Novinha. Foremost among them was that Marcos was incapable of having children, and Novinha's children are offspring of Libo. This is devastating news to Miro, because it means his girlfriend Ouanda is his half-sister. Sanctions from the Intergalactic Congress are learned of and Ender recommends that the colony declare itself in rebellion. He re-establishes contact with Jane who masks their ansible signal.
He enters into the beginnings of a relationship with Novinha. His sister, Valentine, agrees to travel to the colony. On the far side of the planet he has discovered a site reminiscent of a dream in Enders Game. With her guidance, he plants the Hive-Queen's pupa in preperation for the rebirth of the Formics after 3000 years.
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