I've create a pydev project in eclipse. 
At the top level of my workspace I can see these two files:
.project
.pydevproject
I can also see these in each of my subfolders that contain my actual projects.
At the top of my workspace there is also a 
.metadata. folder.
What should I commit to source control?
Ie what can I delete and still be able to open the project with minimal effort (hopefully entirely automated regeneration of files)? If this was Visual Studios C++ project the answer would be to keep just the ".sln", "vcxproj" and "vcxproj.filters" because the "vs" folder and "suo" files will autogenerate on openning. I've tried to delete the ".metadata" folder, but after that nothing appears to load in my workspace.
Also, I am working with someone not using an IDE. What eclipse files do we need to update to keep in sync?
Disclaimer: I am not familiar with PyDev, just with Eclipse in general. You definitely should not check in the .metadata folder. That one is for your Eclipse workspace as a whole and contains your personal configuration. (That's why your workspace appeared empty after you deleted that folder.) In fact, you should not check in your workspace folder at all, but just the several project folders within it.
Whether to check in the .project files is sort of a matter of taste. Those contain project specific information and settings and with those its easier to import the project into Eclipse, but you can import the project without those, too, it's just a bit more work. If other developers are not using Eclipse, those are useless for them. In the worst case, your co-developers will delete those files from source control and when you update your project later, they are deleted on your end, too, messing up your project.
About deleting the files: Note that there is a difference between not checking files into version control and deleting them locally. So in short: Do not commit those files into version control, but don't delete them locally, either. Depending on what sort of version control you are using, you can set it to ignore those files.
What to commit to source control in Eclipse Pydev