I'd say it depends on the mechanism you are using.
I've seen a general style of automated system, many of them based of the same product - where you essentially build yourself an account and a profile, then submit your interest in certain jobs in the company's listing. It's not a size-of-company thing, it's just the interface - although I'd assume it costs enough that a very, very small company may not ever want to spend that kind of money...
In any system this abstract, I'd say it's worth it to apply for any job that interests you. The company will see your resume and note the interest in multiple jobs. Given that there's this system controlling it all, I doubt it will cause much chaos.
If you ever go through personal connections, the first recommendation is to get the skinny from your connections. Job description writing is an abstract art form, and the insights from a friend can be invaluable. Do that first, and if you really are still interested in both options equally, go with your contact's guidance.
Writing to the Opportunity
If you're doing this in a more traditional formal, write a cover letter connecting the dots. Generally you can say in that letter why you like both options and what you want in a job overall, so that the person receiving your application can figure out what to do with you.
Behind the scenes
Generally, a company recruits by having someone inside or outside of the company take responsibility for finding candidates, screening them, introducing them to the process, and advocating for appointments with internal decision makers. To keep ownership clear, it's typical that the recruiter is responsible for some collection of open positions.
So - the big thing behind the scenes is whether both opportunities are staffed by one person or two. And if it's 2, how well they communicate. With one person, anything you can do to connect the interest in both positions is a good thing - like a cover letter. With two people, it's likely that your best interest is served by applying both places, and mentioning that you've done so whenever you get a call back on one of them. Hopefully the recruiters know each other well enough to keep each other in the loop, but that's not a given.