Not so local: the population genetics of convergent adaptation in maize and teosinte

Abstract

What is the genetic architecture of local adaptation and what is the geographic scale that it operates over? We investigated patterns of local and convergent adaptation in five sympatric population pairs of traditionally cultivated maize and its wild relative teosinte (Zea mays subsp. parviglumis). We found that signatures of local adaptation based on the inference of adaptive fixations and selective sweeps are frequently exclusive to individual populations, more so in teosinte compared to maize. However, for both maize and teosinte, selective sweeps are frequently shared by several populations, and often between the subspecies. We were further able to infer that selective sweeps were shared among populations most often via migration, though sharing via standing variation was also common. Our analyses suggest that teosinte has been a continued source of beneficial alleles for maize, post domestication, and that maize populations have facilitated adaptation in teosinte by moving beneficial alleles across the landscape. Taken together, out results suggest local adaptation in maize and teosinte has an intermediate geographic scale, one that is larger than individual populations, but smaller than the species range.

Large haplotypes highlight a complex age structure within the maize pan-genome

“…On average, two alleles will coalesce to their most recent common ancestor after 2 Ne generations. Three prior estimates of historical Ne suggest a minimum Ne for maize of ∼6,000 (Beissinger et al 2016), a decreasing Ne starting at ∼50,000 and declining to ∼1000 during domestication (Wang et al 2017), and a decreasing Ne starting at about ∼100,000 and declining to ∼10,000 during domestication (Tittes et al 2021). All prior analyses were carried out using short-read alignments.…”

Using genome scans to identify genes used repeatedly for adaptation

“…Identifying repeated adaptation requires an understanding of orthology and paralogy among the lineages being compared. The recent studies of repeated adaptation by Bohutínská et al (2021) and Tittes et al (2021) analyzed species or lineages that were closely enough related that a single reference genome was suitable for all samples. Using a single reference genome for all samples makes identifying loci that exhibit repeated adaptation fairly straightforward, but there are potential complications.…”

“…Various forms of repeated adaptation are increasingly discussed in the population genomics literature, where the same genes or genomic regions are implicated in bouts of adaptation in distinct lineages (e.g. Yeaman et al 2016; Rennison et al 2019; Bohutínská et al 2021; Tittes et al 2021; Rennison and Peichel 2022). However, it is important to note that distinct selection regimes can give rise to a pattern of repeated adaptation.…”

“…With lists of adaptation candidates for each lineage, the overlap among these lists is tested to determine whether it exceeds some null expectation. Such overlap methods have revealed some interesting evolutionary patterns in recent studies; for example, Bohutínská et al (2021) showed that the extent of repeated adaptation was related to genetic distance among lineages, and Tittes et al (2021) showed that repeated adaptation between maize and teosinte is often facilitated by the migration of alleles across populations. While these methods yield insights into genome-wide patterns of repeated adaptation, they do not provide statements of confidence about the importance of individual genes.…”

Impacts of pleiotropy and migration on repeated genetic adaptation

“…Previous models provide expectations for the contribution of pleiotropy and effect size to repeatability in isolated populations, however the interaction of these parameters with gene flow in locally-adapting populations has not been studied. This stands in contrast to the growing body of empirical work describing repeatability in locally-adapting populations and divergent lineages with gene flow [1][2][3][4]. To provide a theoretical grounding for such studies, we utilize individualbased simulations of quantitative trait evolution examining how the interplay between inter-locus heterogeneity in pleiotropy and migration-selection balance affects genetic convergence.…”