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Chief Rufus Copage of Shubenacadie (Indian Brook) First Nations, N.S., carries the Assembly of First Nations Eagle Staff during the grand entry as First Nations leaders, elders, youth and delegates gather for the Assembly of First Nations Special Chiefs Assembly in Ottawa on Tuesday, May 27, 2014.Sean Kilpatrick/The Canadian Press

The new head of the Assembly of First Nations who will be elected this week in Winnipeg may see the organization transformed into a formidable opponent of government. Or he may preside over its decline to irrelevance.

The notion that one advocacy group could effectively represent the interests of more than 600 First Nations was ambitious even 30 years ago, when the AFN was created. Today, the role of national chief is more difficult than ever.

That may help explain why just three people – all men – are campaigning for the position. They are Perry Bellegarde and Ghislain Picard, two veterans of the AFN executive, and outsider Leon Jourdain.

In July, 2011, when the last leadership assembly was held, eight names were on the ballot. But much has taken place since to fracture the already strained relationship between the federal government and the First Nations.

A failed attempt to restructure and refinance education on reserves resulted in the resignation of former national chief Shawn Atleo. A breakaway group of chiefs tried to create a new First Nations alliance to rival the AFN.

Several contentious bills were passed into law by the Conservative government of Prime Minister Stephen Harper over the objections of First Nations people. And changes to environmental legislation led to the rise of Idle No More, a loosely knit grassroots protest group that publicly questioned whether native leaders were doing their jobs and whether the organization can continue to have relevance.

"If there is one thing that the Harper government has been successful at, it has been really shining a bright light on the old boys club of the Assembly of First Nations," says Clayton Thomas-Muller, an organizer with Idle No More.

Some say the lines of dialogue with the federal government must remain open despite the acrimony.

Mr. Bellegarde is one of them. Without conversation, he asks, how can the two sides ever understand each other?

Mr. Picard has said he does not see the point in engaging with a government he described as the common enemy of First Nations people. But, he says, discussions that do take place must be conducted on native terms.

And Mr. Jourdain says he would simply not embarrass his people by having them beg at the federal table.

All of which could spell three fractious years ahead for a government that is intent on developing resources on and through First Nations territory.

Some chiefs who will vote for the AFN leader this week oppose a combative approach. Indeed, the hard-liners did not get far in the ballots for national chief in 2011, when Mr. Atleo was elected for a second term.

Roger Augustine, the AFN regional chief for New Brunswick, says the AFN leader's most important task is improving relationships with governments, both federal and provincial. And that requires direct negotiation, he says.

But any national chief who engages in such talks will be labelled a "conciliator," Mr. Augustine says. That is now a dirty word in First Nations politics. So "the next national chief," he says, "will have the toughest time ever in the history of the Assembly of First Nations in attempting to please everyone or to walk the middle of the road."

Not only will he have to play to very different factions within the First Nations, he will have to oversee a reform of the organization itself.

There is broad agreement that the AFN can no longer rely as heavily on federal funds for its operations. But where else can the money be found?

And there is an understanding that the group must be more responsive to the people on the ground. But how can that be done without turning what is now just an advocacy group into another layer of government?

"We are in a very interesting time in Canadian history, and I think that First Nations find themselves at the forefront of it," says Mr. Thomas-Muller. "Whoever the national chief is, they are going to have to deal with some very hard truths. And they can either go ahead and use the prescription of the old boys club and try to maintain the status quo. Or they can be far more radical and ambitious and do something that is supported by the people."

By the numbers

901,000

Number of people in Canada represented by the AFN, almost evenly divided between those who live on and off reserves. First Nations is the largest of three distinct groups recognized as aboriginal by the Constitution Act of 1982. The other two are Inuit, with a population of about 50,000, and Métis, with a population of about 400,000.

617

Number of First Nations communities across Canada, according to the federal aboriginal affairs department. The AFN says there are 634. They represent more than 50 distinct nations and language groups. Each First Nation gets a single vote for the national chief.

10

Number of AFN regional chiefs. They represent the regions of British Columbia, Alberta, Saskatchewan, Manitoba, Ontario, Quebec and Labrador, Nova Scotia and Newfoundland, New Brunswick and Prince Edward Island, Northwest Territories, and Yukon Territory.

3 years

Usual frequency of elections for the national chief. The winner of this week's election will serve for three-and-a-half years to allow the next leadership assembly to take place during the summer, when such meetings have traditionally been held.

Sources: AFN, Métis Nation, Aboriginal Affairs and Northern Development Canada, Statistics Canada

Editor's note: The Métis population of Canada is about 400,000. An earlier version of this story said there were 40,000.