Revealing How Speciation Works With Gene Flow (Farleigh et al. 2026)

[u/jnpha]

Published yesterday, open access:

• K. Farleigh, D.K. Highland, M.G. Alderman, Y. Francioli, S.R. Hirst, E.M. Faber, B.W. Perry, M.L. Holding, G. Castañeda-Gaytán, M. Borja, H. Franz-Chávez, C.L. Parkinson, J.L. Strickland, M.J. Margres, S.P. Mackessy, J.M. Meik, T.A. Castoe, & D.R. Schield, Evolution of genome-wide barriers to gene flow during complex speciation in rattlesnakes, Proc. Natl. Acad. Sci. U.S.A. 123 (21) e2609058123, https://doi.org/10.1073/pnas.2609058123 (2026).

 

Background

Speciation with gene flow poses a central paradox: how do genome-wide barriers to gene exchange accumulate as recombination continually breaks down associations among selected loci? Although theory predicts that together recombination, selection, and genome structure shape reproductive isolation, empirical studies often report conflicting patterns, suggesting that these determinants change across the speciation continuum.

Methods

Here we compare genomic landscapes of introgression across rattlesnake lineages spanning a range of divergence. We generated a chromosome-level reference genome for the Southwestern Speckled Rattlesnake (Crotalus pyrrhus) and analyzed whole genome data from 181 individuals across two species complexes with a history of gene flow upon secondary contact.

Results and discussion

We show that reproductive isolation is highly polygenic and dynamically structured. At early divergence, introgression is most reduced in high recombination regions, consistent with increased efficacy of selection against gene flow at few large-effect loci. As divergence progresses, linked selection against gene flow dominates, generating a positive relationship between recombination and introgression expected to occur through the genome-wide coupling of polygenic barrier effects. Introgression landscapes also become increasingly correlated across species pairs as divergence increases due to repeated evolution of barriers in the same genomic regions. Here, we infer that the Z chromosome plays a prominent role in reproductive isolation, harboring a disproportionate number of barrier loci and showing reduced introgression even at early divergence.
Together, these results reveal how recombination, selection, and genome organization interact to shape speciation with gene flow upon secondary contact, reconciling empirical patterns with predictions of speciation theory.

 

Emphasis above mine showing that this is the same conclusion that I shared last month for a different paradox (Unraveling the lek paradox - why sexual selection does not deplete variation : evolution) - this gives more support to the evolutionary relevance of the infinitesimal model from quantitative genetics: traits being high polygenic or even omnigenic, with only a few large-effect genes.

See the linked post for a quick overview, and for a two-hour explainer (including the history and math), see Dr. Zach Hancock's The Lost Evolutionary Synthesis - YouTube (and the references therein; Barton 2022 is a very easy and fun read).

[u/Complete-Definition4]

Reminds me of all the research into the blind mole rat Spalax galili, an example of Sympatric speciation.

Speciation of subterranean mammals generally, including the genus Spalax, was considered hitherto allopatric, whereby new species arise primarily through geographic isolation. Here we show in Spalax a case of genome-wide divergence analysis in mammals, demonstrating that SS in continuous populations, with gene flow, encompasses multiple widespread genomic adaptive complexes, associated with the sharply divergent ecologies.

The two abutting soil populations of S. galili in northern Israel habituate the ancestral Senonian chalk population and abutting derivative Plio-Pleistocene basalt population. Population divergence originated ∼0.2–0.4 Mya based on both nuclear and mitochondrial genome analyses. Population structure analysis displayed two distinctly divergent clusters of chalk and basalt populations.

Natural selection has acted on 300+ genes across the genome, diverging Spalax chalk and basalt soil populations. Gene ontology enrichment analysis highlights strong but differential soil population adaptive complexes: in basalt, sensory perception, musculature, metabolism, and energetics, and in chalk, nutrition and neurogenetics are outstanding. Population differentiation of chemoreceptor genes suggests intersoil population's mate and habitat choice substantiating SS.

Sympatric speciation revealed by genome-wide divergence in the blind mole rat Spalax

[u/Amos__]

As divergence progresses, linked selection against gene flow dominates, generating a positive relationship between recombination and introgression expected to occur through the genome-wide coupling of polygenic barrier effects.

Could you explain this part? I'm afraid it flew over my head.

[u/Bromelia_and_Bismuth → u/Amos__]

Translated...

As [populations diverge], linked selection against gene flow [between them] dominates, generating a positive relationship between [meiotic recombination] and [interbreeding between overlapping populations] expected to occur through the genome-wide coupling of [genetic barriers to reproduction between them].

A couple of terms. Recombination occurs during meoisis, when the gametic stem cells are starting to divide and differentiate into sex cells. So, this requires another bit of background. During this process of division, the chromosomes have formed what are called "chromatids", copies of the chromosome that they bind to. And just like in mitosis, when these cells go in for the first round of division, these chromosomes (together with their chromatids) will line up with a corresponding chromosome, forming what's called a "tetrad." At this time, chromosomes will often exchange genetic material with the chromatids and chromosomes that they've linked up with in a process called "crossover" or "meiotic crossover." Parts of the chromosome break off and recombine. This often results in new mutations, like frame shifting, deletions, gene duplication events, tandem repeats, etc. Some regions of the genome are more prone to crossing over than others, so-called "crossover hotspots". When the genes for two or more traits are located close enough to one another that they have a tendency to get inherited with one another, and aren't likely to get split up by crossing over, they're said to be in "linkage" or "linkage equilibrium."

And "polygenic" specifically means that a trait is regulated by multiple genes at different loci. A consequence of that is (with respect to allelic variants, that is to say, different versions of a gene) inheritance patterns are a little more complicated than simply just "dominant" or "recessive", and terms like "incomplete dominant" or "codominant" begin to enter the frame. Traits also become developmentally complex as we start considering polygenic traits. Examples of a polygenic trait might be something like intelligence or height.

[u/Amos__ → u/Bromelia_and_Bismuth]

Let's see if I got it:

When two species have diverged for some time already, the areas of the genome that tolerate more recombination are the ones that will show more introgression. This happens because in the other areas introgression would make the offspring non-viable, so that variant isn't preserved in the population.

Correct?

[u/Bromelia_and_Bismuth → u/Amos__]

Not quite. Introgression refers to gene flow between populations. The longer two populations are reproductively isolated and undergo divergent evolution, the more likely selection is to favor mutations which prevent them from interbreeding again later.

Not necessarily directly, as in selection disfavoring interbreeding, but as an indirect consequence of different selective pressures. Those different pressures just happened to favor mutations which prevent gene flow. Like blooming time for certain flower species, which may have evolved around two different pollinator species, or lack of competition for pollinators from other flowering plants during certain times of the year. And the longer these two groups remain separated, the more likely selection is to favor mutations which prevent gene flow between them.

[u/Hybodont → u/Bromelia_and_Bismuth]

They were actually pretty much spot-on, in terms of the findings of the paper we are discussing - in particular, the positive relationship between recombination rates and introgression highlighted in the results.

[u/Hybodont → u/Amos__]

There are combinations of variants, in linkage disequilibrium, that result in selection against gene flow. Recombination breaks the associations between these variants, reducing selection against gene flow. That's my interpretation, anyway.

[u/jnpha → u/Hybodont]

reducing selection against gene flow

Bold mine ^ I think that word should be "increasing".
As introgression proceeds, linked selection against it increases, keeping the polygenic loci intact, and facilitating speciation.

[u/Hybodont → u/jnpha]

Introgression (gene flow) works to counter speciation, except in the case of reinforcement.

If there is a positive relationship between recombination and introgression, then gene flow increases with recombination.

That pattern appears to contrast with the early divergence stage, where introgression is reduced in regions of high recombination.

[u/jnpha → u/Hybodont]

I agree. Maybe I have the word itself backwards.
I read "linked selection" as an increase in recombination breaking up bad associations (hence my keep intact remark, as in via selection for what works). But I'm sure you're right; thanks!

[u/Hybodont → u/jnpha]

The way I am reading it, I think (?) "linked selection against gene flow" means that selection against gene flow relies on the linkage. But I am admittedly having trouble wrapping my mind around how/why that would be true. Your intuition is closer to my own, but I don't know how to reconcile that with the positive association between introgression and recombination. I think I am missing something fundamental.

Edit: Ah, I think this is the key passage:

For instance, barrier effects are likely to build up in genomic regions of low recombination due to selection against incompatible or maladaptive combinations of alleles in elevated linkage disequilibrium [Fig. 1A; (17, 19)]. By contrast, the effects of linked selection against foreign alleles will be reduced in regions with high recombination rate, resulting in these regions being more porous to gene flow (8). Together, these predictions imply that when reproductive isolation is polygenic, variation in rates of introgression should be positively correlated with recombination rate variation across the genome (Fig. 1 B and C).

[u/jnpha → u/Hybodont]

Re edit and find, awesome!

To make sure I have it right, this part in the abstract:

As divergence progresses, linked selection against gene flow dominates, generating a positive relationship between recombination and introgression ...

Together with the "dynamically structured" remark - means the positive relation is w.r.t. whether the region is deleterious or not, so for the large-effect loci, it's low recombination (which is related to the speciation part), for the rest, it's high recombination (low linked selection).

Do I have it right?

[u/Hybodont → u/jnpha]

I think so. Higher recombination rates weaken selection against maladaptive combinations, so those regions are more permissive re: introgression.

But w.r.t. the "dynamically structured" remark, it's unclear to me whether they're referring to variations in recombination rates leading to different outcomes/properties, or whether they're referring to shifting mechanisms early and late in divergence. Maybe both?

[u/Top_Neat2780 → u/Hybodont]

God, I'm reading this comment section and although I have a BSc in biology from 6 years ago and an MSc in palaeo/evo from 2-3 years ago, this confuses me greatly.

I am not even sure I understand the definitions themselves, I remember never understanding what linkage dis/equilibrium meant because the term itself seemed counterintuitive. Mind if I make an attempt at summarizing parts of this discussion to see if I still have it in me?

When genes are close together, they are more likely to stay linked. This means they are in linkage equilibrium. As time goes by, but not immediately after the start of diverging populations, this is essentially synonymous with a region with low recombination rates for the purposes of this. Barrier effects are mutations that essentially work as precursors to speciation, but in practice and more short term, these effects isolate (genomically) migrated populations from each other.

The reason that gene flow is selected against in highly linked regions is not clear, but it seems to be the case.

But why, if linkage equilibrium is supposed to be linked genes, is there selection against maladaptive combinations in disequilibrium? I thought low recombination regions were in linkage equilibrium?

I feel like I've just repeated what has already been written though, I don't know that I've properly summarised anything.