De Villiers has yet to feature in a 2015 test, having undergone major knee surgery after being injured against Wales last November.
The 34-year-old's return comes as a huge boost for coach Heyneke Meyer ahead of the September-October World Cup in England with De Villiers' leadership both on and off the pitch valued highly.
As a result of his inclusion at outside centre, explosive prospect Jesse Kriel will move to right wing.
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"Jean's comeback is truly remarkable and very inspirational and I can't wait to see what he can offer playing next to exciting youngsters such as (flyhalf) Handre Pollard, (inside centre) Damian (De Allende) and Jesse," Meyer said in a news release on Wednesday.
"Jean now has 160 minutes of rugby behind him since his comeback a month ago and I'm very satisfied that he will be able to make his mark as player and captain."
The forwards on the bench are again rotated due to injuries, with flank Siya Kolisi and lock Pieter-Steph du Toit returning as replacements. Neither have played a test since the victory over France in Paris in late 2013.
The other changes to the team are all also injury-enforced after South Africa's bruising 27-20 loss to New Zealand at Ellis Park late last month ruled them out of contention for this year's championship.
Flanker Marcell Coetzee returns and will take over from Francois Louw, while prop Vincent Koch will get his first start for the Boks in place of Jannie du Plessis.
Marcel van der Merwe (prop) has been named on the bench for his first test of 2015, while wing Lwazi Mvovo is also among the replacements.
Meyer said that although scrumhalf Fourie du Preez and flank Willem Alberts started training with the squad this week, they would be given more time to fully recover from their respective injuries.
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Team: 15-Willie le Roux, 14-Jesse Kriel, 13-Jean de Villiers (captain), 12-Damian de Allende, 11-Bryan Habana, 10-Handre Pollard, 9-Ruan Pienaar, 8-Schalk Burger, 7-Marcell Coetzee, 6-Heinrich Brussow, 5-Lood de Jager, 4-Eben Etzebeth, 3-Vincent Koch, 2-Bismarck du Plessis, 1-Tendai Mtawarira
Replacements: 16-Adriaan Strauss, 17-Trevor Nyakane, 18-Marcel van der Merwe, 19-Pieter-Steph du Toit, 20-Siya Kolisi, 21-Cobus Reinach, 22-Pat Lambie, 23-Lwazi Mvovo
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