Cooperation mitigates diversity loss in a spatially expanding microbial population

The evolution and potentially even the survival of a spatially expanding population depends on its genetic diversity, which can decrease rapidly due to a serial founder effect. The strength of the founder effect is predicted to depend strongly on the details of the growth dynamics. Here, we probe this dependence experimentally using a single microbial species, Saccharomyces cerevisiae, expanding in multiple environments that induce varying levels of cooperativity during growth. We observe a drastic reduction in diversity during expansions when yeast grows noncooperatively on simple sugars, but almost no loss of diversity when cooperation is required to digest complex metabolites. These results are consistent with theoretical expectations: When cells grow independently from each other, the expansion proceeds as a pulled wave driven by growth at the low-density tip of the expansion front. Such populations lose diversity rapidly because of the strong genetic drift at the expansion edge. In contrast, diversity loss is substantially reduced in pushed waves that arise due to cooperative growth. In such expansions, the low-density tip of the front grows much more slowly and is often reseeded from the genetically diverse population core. Additionally, in both pulled and pushed expansions, we observe a few instances of abrupt changes in allele fractions due to rare fluctuations of the expansion front and show how to distinguish such rapid genetic drift from selective sweeps.

Cooperation mitigates diversity loss in a spatially expanding microbial population

The evolution and potentially even the survival of a spatially expanding population depends on its genetic diversity, which can decrease rapidly due to a serial founder effect. The strength of the founder effect is predicted to depend strongly on the details of the growth dynamics. Here, we probe this dependence experimentally using a single microbial species, Saccharomyces cerevisiae, expanding in multiple environments that induce varying levels of cooperativity during growth. We observe a drastic reduction in diversity during expansions when yeast grows non-cooperatively on simple sugars, but almost no loss of diversity when cooperation is required to digest complex metabolites. These results are consistent with theoretical expectations. When cells grow independently from each other, the expansion proceeds as a pulled wave driven by the growth at the low-density tip of the expansion front. Such populations lose diversity rapidly because of the strong genetic drift at the expansion edge. In contrast, diversity loss is substantially reduced in pushed waves that arise due to cooperative growth. In such expansions, the low-density tip of the front grows much more slowly and is often reseeded from the genetically diverse population core. Additionally, in both pulled and pushed expansions, we observe a few instances of abrupt changes in allele fractions due to rare fluctuations of the expansion front and show how to distinguish such rapid genetic drift from selective sweeps.Significance statementSpatially expanding populations lose genetic diversity rapidly because of the repeated bottlenecks formed at the front as a result of the serial founder effect. However, the rate of diversity loss depends on the specifics of the expanding population, such as its growth and dispersal dynamics. We have previously demonstrated that changing the amount of within-species cooperation leads to a qualitative transition in the nature of expansion from pulled (driven by migration at the low density tip) to pushed (driven by migration from the high density region at the front, but behind the tip). Here we demonstrate experimentally that pushed waves, which emerge in the presence of sufficiently strong cooperation, result in strongly reduced genetic drift during range expansions, thus preserving genetic diversity in the newly colonized region.

Can a linguistic serial founder effect originating in Africa explain the worldwide phonemic cline?

It has been proposed that a serial founder effect could have caused the present observed pattern of global phonemic diversity. Here we present a model that simulates the human range expansion out of Africa and the subsequent spatial linguistic dynamics until today. It does not assume copying errors, Darwinian competition, reduced contrastive possibilities or any other specific linguistic mechanism. We show that the decrease of linguistic diversity with distance (from the presumed origin of the expansion) arises under three assumptions, previously introduced by other authors: (i) an accumulation rate for phonemes; (ii) small phonemic inventories for the languages spoken before the out-of-Africa dispersal; (iii) an increase in the phonemic accumulation rate with the number of speakers per unit area. Numerical simulations show that the predictions of the model agree with the observed decrease of linguistic diversity with increasing distance from the most likely origin of the out-of-Africa dispersal. Thus, the proposal that a serial founder effect could have caused the present observed pattern of global phonemic diversity is viable, if three strong assumptions are satisfied.

A comparison of worldwide phonemic and genetic variation in human populations

Worldwide patterns of genetic variation are driven by human demographic history. Here, we test whether this demographic history has left similar signatures on phonemes—sound units that distinguish meaning between words in languages—to those it has left on genes. We analyze, jointly and in parallel, phoneme inventories from 2,082 worldwide languages and microsatellite polymorphisms from 246 worldwide populations. On a global scale, both genetic distance and phonemic distance between populations are significantly correlated with geographic distance. Geographically close language pairs share significantly more phonemes than distant language pairs, whether or not the languages are closely related. The regional geographic axes of greatest phonemic differentiation correspond to axes of genetic differentiation, suggesting that there is a relationship between human dispersal and linguistic variation. However, the geographic distribution of phoneme inventory sizes does not follow the predictions of a serial founder effect during human expansion out of Africa. Furthermore, although geographically isolated populations lose genetic diversity via genetic drift, phonemes are not subject to drift in the same way: within a given geographic radius, languages that are relatively isolated exhibit more variance in number of phonemes than languages with many neighbors. This finding suggests that relatively isolated languages are more susceptible to phonemic change than languages with many neighbors. Within a language family, phoneme evolution along genetic, geographic, or cognate-based linguistic trees predicts similar ancestral phoneme states to those predicted from ancient sources. More genetic sampling could further elucidate the relative roles of vertical and horizontal transmission in phoneme evolution.