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On a losing football team, the backup quarterback is often the most popular guy in town. The flaws of the starter are picked apart by a skeptical public, while the backup’s virtues become magnified by comparison.

So it’s no surprise to hear people clamoring for Thad Lewis, who has done a serviceable job this season as the No. 2 man to rookie EJ Manuel. Lewis has beaten the Dolphins twice, which elevated him to the saintly level of Frank Reich in the eyes of desperate Bills fans.

Lewis is a decent player, though turnover-prone. He throws a nice ball and is willing to take chances downfield. That goes a long way with fans, many of whom feel Lewis is better than Manuel right now – or at the very least, no worse an option at this stage of their careers.

I’m not here to debate Lewis vs. Manuel. The fact is, Manuel is the starter, the QB with the greater upside, the man the Bills are desperately hoping can evolve into a genuine franchise guy and lead them to the playoffs in the near future.

The question is what the Bills should do at No. 2 next season. They need to do better than Lewis and Jeff Tuel, who are both marginal NFL quarterbacks. If they’re serious about making a playoff run in 2014, they need a reliable veteran to serve as Manuel’s backup.

Doug Whaley did a good job supplementing the roster in his first season as general manager. He brought in Jerry Hughes and Manny Lawson to bolster his linebacking corps. Both performed well above expectations.

Whaley brought in Kevin Kolb to compete with Manuel for the No. 1 quarterback job. His big mistake was not finding a more capable backup when Kolb suffered a concussion and was lost for the year.

The Bills compounded the blunder by giving the backup job to Tuel, who proved to be over his head. It might have cost them the Cleveland game, when Tuel fell on his face after replacing Manuel, and the Kansas City game, when Tuel had to start in Lewis’s stead.

They can’t make the same mistake again. Manuel is the presumed starter next season. He is still very raw, and the Bills will be patient with him. But they need to have a better relief option in the event that Manuel regresses to an unsupportable degree, or he gets hurt again.

The kid gloves will be off next season. If Manuel shows progress, the way Ryan Tannehill did in his second year for Miami, things will be fine. But if he stumbles and has a couple of stinkers like he did on the road this season, it will be troubling, indeed.

It happened in 2005, remember, when J.P. Losman was handed the starting job and faltered badly early in the season. A number of veterans began mumbling. They felt an inferior young QB was compromising their chance to make the playoffs late in their careers.

Losman lost his job to Kelly Holcomb, a capable if unremarkable veteran who gave the Bills a better chance to win games in the short term. It didn’t pay dividends, but when there’s a political firestorm inside the locker room, it can prod a coach into making a change.

I’m not saying Manuel is J.P. Losman. Manuel is a smarter and more poised young quarterback who should improve as he goes along. And unlike Losman, he’ll go into his second year with 10 – or 11, if he plays Sunday – games as a starter under his belt.

But the Bills need to prepare for the worst. Now that Manuel has suffered three knee injuries in four months, it’s more vital than ever to have an established second option. It would be irresponsible to have a marginal NFL quarterback like Lewis or Tuel as the No. 2 guy.

There are no more excuses for this team. They weren’t that far away this season, despite their youth at quarterback and their various injuries.

If a season in which a single play could have decided four games, an experienced quarterback could have made a world of difference.

The Bills wasted some great defense this season. The D let them down on numerous occasions, true, but the lack of a reliable passing game was the biggest problem. Strong quarterback play would make all those gaudy defensive numbers a lot more meaningful.

There’s a strong leadership core on this team – starting with Fred Jackson and Kyle Williams, two tough, principled veterans who arrived here in 2006 and have never played on a winner.

Both Williams and Jackson are nearing the end of their careers. They’re unselfish team players, examples for the younger guys to follow. But even they might get resentful if a struggling young quarterback was holding them back from that long-awaited chance at the postseason.

The market for quarterbacks won’t be great. The Bills won’t go after Michael Vick or Jay Cutler, high-priced vets who would pose a threat to Manuel. They still have the rights to Kolb, but the chances of him ever returning to the NFL aren’t good after four concussions.

There are a number of solid if uninspiring possibilities, experienced veterans who could be trusted to be a backup and mentor to Manuel:

Chad Henne and Matt Cassel have started and been in the league at least six years. Matt Schaub, who might be let go after a rough year in Houston, might be cut loose by the Texans.

Hey, they could take another run at Tarvaris Jackson or Matt Flynn, who never had sufficient opportunity to master the profoundly complex offensive systems of the coaches here in Buffalo.

Chances are, Manuel will play well enough to remain the starter and keep the Bills in the playoff race next season.

If the defense is better in its second year under Mike Pettine, it’s hard to imagine them not being competitive in almost every game again.

Suppose they’re 7-5, tied for a playoff spot, and Manuel hurts his knee with a month left to go in the season. Do you want the offense in the hands of Thad Lewis down the stretch, with the first playoff berth in 15 years on the line? Or for that matter, Jeff Tuel?

That’s the question Whaley, Marrone and the fellows will be asking themselves in the months ahead. I know what my answer would be.

email: jsullivan@buffnews.com