Hey All,

This is a paper based on my dissertation research and is coming out in Evolution, currently available as early view on the journal's website. It describes extensive mitochondrial replacement in Redline Darters, Nothonotus rufilineatus, where all N. rufilineatus in the Cumberland River Drainage have Nothonotus camurus-like mitochondria and most N. rufilineatus from the Flint R. and upstream in the Tennessee River Drainage have Nothonotus chlorobranchius-like mitochondria, as well as N. rufilineatus acting as a 'conduit species' by transferring N. chlorobranchius-like mitochondria to N. camurus. This isn't the first time mitochondrial replacement has been documented in darters, but it is the first time replacement has occurred between different species in different systems and included a conduit species.

Ben

 Keck&Near2010.pdf   892.53KB   46 downloads

I haven't thoroughly read the whole article yet (famous last words) but it's a funny finding that most redline populations you examined don't have redline mtDNA, from looking at Table 1. Maybe we can safely say that most Nothonotus species can be expected to have Nothonotus mitochondria?

Your Conclusion begins with the statement that mitochondrial replacement in these species as well as other vertebrates "provides insights into the failure of reproductive isolating barriers in vertebrates". That raises all sorts of interesting questions, from the ever-popular how does one define a species, to molecular and behavioral mechanisms that may or not be rigid enough to truly separate closely related species. And the finding that redlines may be a conduit for mtDNA between other Nothonotus is truly sublime in its weirdness.

Hello Bruce, As the coauthor of Ben's paper I will chime in. Indeed, based on Ben's extensive work with Nothonotus, it seems that there are no Nothonotus species that have captured mtDNA from Ammocrypta, Etheostoma, or Percina species/lineages. This mtDNA transfer is something that is not unique to Nothonotus. It has been observed in Etheostoma and Percina. I do not think it reflects on the "species" status of these lineages, as reproductive barriers are quite strong for autosomal genes, but the species boundaries are leaky when it comes to mitochondrial genomes.

Yeah, I understand that from other recent work by your group. Understanding the mechanism(s) that allow for common mtDNA movement, but usually not nuclear genes, is the part that fascinates me because as you and Ben mention in this paper it raises questions about different male dispersal rates in different species. And as such it raises questions about variability in sexual selection processes between closely and not so closely related species. Obviously females of some these species find males of other species perfectly attractive under at least some circumstances.

I have a printed copy of the paper with me so I'll read it in its entirety...

Bruce, There is another aspect that we have not assessed. That is the potential selective advantage of the "foreign" mtDNA genome. This would put the spread of the introgressed mtDNA into a context that would trump sexual selection, etc.

You're right, that's a possibility too. It's looking at the tension between sexual and natural selection; is it that male redlines are more attractive and maybe make better fathers, maybe produce more and higher quality sperm per unit (sperm competition may be underappreciated in fish)? Is there something about the mtDNA genes from the other species that enhance some aspect of aerobic respiration? Or, the list of possibilities could be bigger. Either way it's a fascinating story worthy of follow-up on several levels.

Hey Bruce!

This was the first part, the description of the pattern, and now it's on to figuring out why we see this pattern. As you've pointed out the list of possible causes is extensive. The great thing is that "We have the technology" to test most of the things mentioned. I have a feeling it's got lots to do with sneaking males (male biased dispersal) and that some mtDNA lineages confer an advantage in certain habitats. Different sperm motility between the species is also something we need to look at and is something we alluded to in our recent Copeia paper, stating that ~1% of darter species have been studied for this. Lots of experiments, lots of field work, lots of fun.... and as usual, need more funding.

Ben

In multi-Notho assemblages, is there any (I'm assuming yes, but also asking a rhetorical question) indication of partition of spawning resources by time/temperature/light? For example, are sneaky males a small percentage of NothoX population that are reporductively active longer than normal, so with no active females of their species they are looking to spread genetic material and NothoY happens to be active near by? Use it or lose it right? Conversley, all the nice cobbles may be taken in typical NothoX habitat, but NothoY habitat is juuuuuuuuuust a short distance away, and male NothoY's are wimps so darting over for a sneak attack (especially if NothoX has more motile sperm) gives you the benefits of transfering genetic material without the effort of fighting for a territory, displaying/courting, etc.

Fascinating stuff guys...

Hey Matt,

Bob Stiles did his graduate research at U Tennessee that included some info on breeding of Nothonotus in the upper TN system and was probably the first to note sneaking male behavior for Nothonotus, it's also been documented in N. camurus but I forget the citation right now. Stiles noted male N. rufilineatus that were pigmented more like females, so say juvenile color with a bit of red on the edges of the fins, were sneaking matings. His notes included some N. rufilineatus X N. camurus spawnings, if I'm remembering right, those were not N. rufilineatus males of that color pigmentation, but it was still male N. rufilineatus. Your questions are all ones that need to be answered with some decent field observation and lab experiments... hopefully we'll be able to get these done as I think this a great model system for documenting reticulate evolution in vertebrates. It may be that the sneaky males are only sneaky males for their first reproductive year, year one probably, and subsequently maintain normal male pigmentation and defend territory, a pattern observed in wrasses. Most Nothos are reproductively active for several months (reportedly April to August)... but that's a species/population average! What hasn't been determined is how long individuals are reproductively active. Are individuals active for the entire period, or are they active for a few days, take a week off, active a few days, etc? I think the latter! I am really hopeful for Todd Crail's work on Nothonotus habitat delimitation to provide some good information on how each Notho uses a stream; I'm just waiting for Todd to publish a nice Winn or Greenburg type manuscript including Nothos, as I'm sure it'll be cited as often as those studies are given his recent talks (yes, that's a challenge Todd). There are soooooo many questions involved with this discovery it's hard to pick just one (or a few) to work on. We are doing what we can and we hope to bring lots of people into the fold to get at the answers. If anyone wants to do their own work with these species we'd be happy to provide any data or tissues we can.

Best, Ben

Hm...I guess I didn't read that part of the theses and just concentrated on the habitat of the sites. I was considering a Greenberg, Crail type study at the time of my MS, specifically large assembalges with FE/SE darters so I poked around those sites a bit. At least I feel a little better about myself when no one believed me that there were some odd looking Nothos in the lower Holston. Very interesting stuff guys, always gets my brain going and I think is so much more engrossing than a lot of other published work IMO.

Edited by ashtonmj, 10 January 2010 - 06:44 PM.

I don't know if anyone else has seen the attached article yet, from the 18 December 2009 issue of Science. It summarizes the efforts and interpretations of the authors to model and understand ecological (sympatric, really) speciation. In particular they develop support for the idea that, "Natural and sexual selection work in concert to achieve local adaptation and reproductive isolation, even in the presence of substantial gene flow." That sounds like the crux of what Ben & Tom have observed with the three Nothonotus species. The authors specifically consider the whole question of how can recently separated species remain separate species even in situations where some regular hybridization occurs. How possible is sympatric speciation, and how can it happen? I don't think there are easy answers here, and this article is certainly a more theoretical model-based approach than what most of us here would undertake. On another level, I look forward to what Ben found last year with his N. chlorobranchius field work.

 vanDoornOnTheOriginOfSpecies.pdf   246.25KB   30 downloads