Joana Meier

Genomics and the origin of species

Speciation is a fundamental evolutionary process, the knowledge of which is crucial for understanding the origins of biodiversity. Genomic approaches are an increasingly important aspect of this research field. We review current understanding of genome-wide effects of accumulating reproductive isolation and of genomic properties that influence the process of speciation. Building on this work, we identify emergent trends and gaps in our understanding, propose new approaches to more fully integrate genomics into speciation research, translate speciation theory into hypotheses that are testable using genomic tools and provide an integrative definition of the field of speciation genomics.

Genomics of Rapid Incipient Speciation in Sympatric Threespine Stickleback

Ecological speciation is the process by which reproductively isolated populations emerge as a consequence of divergent natural or ecologically-mediated sexual selection. Most genomic studies of ecological speciation have investigated allopatric populations, making it difficult to infer reproductive isolation. The few studies on sympatric ecotypes have focused on advanced stages of the speciation process after thousands of generations of divergence. As a consequence, we still do not know what genomic signatures of the early onset of ecological speciation look like. Here, we examined genomic differentiation among migratory lake and resident stream ecotypes of threespine stickleback reproducing in sympatry in one stream, and in parapatry in another stream. Importantly, these ecotypes started diverging less than 150 years ago. We obtained 34,756 SNPs with restriction-site associated DNA sequencing and identified genomic islands of differentiation using a Hidden Markov Model approach. Consistent with incipient ecological speciation, we found significant genomic differentiation between ecotypes both in sympatry and parapatry. Of 19 islands of differentiation resisting gene flow in sympatry, all were also differentiated in parapatry and were thus likely driven by divergent selection among habitats. These islands clustered in quantitative trait loci controlling divergent traits among the ecotypes, many of them concentrated in one region with low to intermediate recombination. Our findings suggest that adaptive genomic differentiation at many genetic loci can arise and persist in sympatry at the very early stage of ecotype divergence, and that the genomic architecture of adaptation may facilitate this.

Demographic modelling with whole-genome data reveals parallel origin of similar Pundamilia cichlid species after hybridization

Modes and mechanisms of speciation are best studied in young species pairs. In older taxa, it is increasingly difficult to distinguish what happened during speciation from what happened after speciation. Lake Victoria cichlids in the genus Pundamilia encompass a complex of young species and polymorphic populations. One Pundamilia species pair, P. pundamilia and P. nyererei, is particularly well suited to study speciation because sympatric population pairs occur with different levels of phenotypic differentiation and reproductive isolation at different rocky islands within the lake. Genetic distances between allopatric island populations of the same nominal species often exceed those between the sympatric species. It thus remained unresolved whether speciation into P. nyererei and P. pundamilia occurred once, followed by geographical range expansion and interspecific gene flow in local sympatry, or if the species pair arose repeatedly by parallel speciation. Here, we use genomic data and demographic modelling to test these alternative evolutionary scenarios. We demonstrate that gene flow plays a strong role in shaping the observed patterns of genetic similarity, including both gene flow between sympatric species and gene flow between allopatric populations, as well as recent and early gene flow. The best supported model for the origin of P. pundamilia and P. nyererei population pairs at two different islands is one where speciation happened twice, whereby the second speciation event follows shortly after introgression from an allopatric P. nyererei population that arose earlier. Our findings support the hypothesis that very similar species may arise repeatedly, potentially facilitated by introgressed genetic variation.

Genomic landscape of early ecological speciation initiated by selection on nuptial colour

Ecological speciation is the evolution of reproductive isolation as a consequence of direct divergent natural selection or ecologically mediated divergent sexual selection. While the genomic signature of the former has been extensively studied in recent years, only few examples exist for genomic differentiation where environment‐dependent sexual selection has played an important role. Here, we describe a very young (~90 years old) population of threespine sticklebacks exhibiting phenotypic and genomic differentiation between two habitats within the same pond. We show that differentiation among habitats is limited to male throat colour and nest type, traits known to be subject to sexual selection. Divergence in these traits mirrors divergence in much older benthic and limnetic stickleback species pairs from North American west coast lakes, which also occur in sympatry but are strongly reproductively isolated from each other. We demonstrate that in our population, differences in throat colour and breeding have been stable over a decade, but in contrast to North American benthic and limnetic stickleback species, these mating trait differences are not accompanied by divergence in morphology related to feeding, predator defence or swimming performance. Using genomewide SNP data, we find multiple genomic islands with moderate differentiation spread across several chromosomes, whereas the rest of the genome is undifferentiated. The islands contain potential candidate genes involved in visual perception of colour. Our results suggest that phenotypic and multichromosome genomic divergence of these morphs was driven by environment‐dependent sexual selection, demonstrating incipient speciation after only a few decades of divergence in sympatry.

Genomics of Parallel Ecological Speciation in Lake Victoria Cichlids

Abstract The genetic basis of parallel evolution of similar species is of great interest in evolutionary biology. In the adaptive radiation of Lake Victoria cichlid fishes, sister species with either blue or red‐back male nuptial coloration have evolved repeatedly, often associated with shallower and deeper water, respectively. One such case is blue and red‐backed Pundamilia species, for which we recently showed that a young species pair may have evolved through “hybrid parallel speciation”. Coalescent simulations suggested that the older species P. pundamilia (blue) and P. nyererei (red‐back) admixed in the Mwanza Gulf and that new “nyererei‐like” and “pundamilia‐like” species evolved from the admixed population. Here, we use genome scans to study the genomic architecture of differentiation, and assess the influence of hybridization on the evolution of the younger species pair. For each of the two species pairs, we find over 300 genomic regions, widespread across the genome, which are highly differentiated. A subset of the most strongly differentiated regions of the older pair are also differentiated in the younger pair. These shared differentiated regions often show parallel allele frequency differences, consistent with the hypothesis that admixture‐derived alleles were targeted by divergent selection in the hybrid population. However, two‐thirds of the genomic regions that are highly differentiated between the younger species are not highly differentiated between the older species, suggesting independent evolutionary responses to selection pressures. Our analyses reveal how divergent selection on admixture‐derived genetic variation can facilitate new speciation events.

The onset of ecological diversification 50 years after colonization of a crater lake by haplochromine cichlid fishes

Adaptive radiation research typically relies on the study of evolution in retrospective, leaving the predictive value of the concept hard to evaluate. Several radiations, including the cichlid fishes in the East African Great Lakes, have been studied extensively, yet no study has investigated the onset of the intraspecific processes of niche expansion and differentiation shortly after colonization of an adaptive zone by cichlids. Haplochromine cichlids of one of the two lineages that seeded the Lake Victoria radiation recently arrived in Lake Chala, a lake perfectly suited for within-lake cichlid speciation. Here, we infer the colonization and demographic history, quantify phenotypic, ecological and genomic diversity and diversification, and investigate the selection regime to ask if the population shows signs of diversification resembling the onset of adaptive radiation. We find that since their arrival in the lake, haplochromines have colonized a wide range of depth habitats associated with ecological and morphological expansion and the beginning of phenotypic differentiation and potentially nascent speciation, consistent with the very early onset of an adaptive radiation process. Moreover, we demonstrate evidence of rugged phenotypic fitness surfaces, indicating that current ecological selection may contribute to the phenotypic diversification.

A Dense Linkage Map of Lake Victoria Cichlids Improved the Pundamilia Genome Assembly and Revealed a Major QTL for Sex-Determination

Genetic linkage maps are essential for comparative genomics, high quality genome sequence assembly and fine scale quantitative trait locus (QTL) mapping. In the present study we identified and genotyped markers via restriction-site associated DNA (RAD) sequencing and constructed a genetic linkage map based on 1,597 SNP markers of an interspecific F2 cross of two closely related Lake Victoria cichlids (Pundamilia pundamilia and P. sp. ‘red head’). The SNP markers were distributed on 22 linkage groups and the total map size was 1,594 cM with an average marker distance of 1.01 cM. This high-resolution genetic linkage map was used to anchor the scaffolds of the Pundamilia genome and estimate recombination rates along the genome. Via QTL mapping we identified a major QTL for sex in a ∼1.9 Mb region on Pun-LG10, which is homologous to Oreochromis niloticus LG 23 (Ore-LG23) and includes a well-known vertebrate sex-determination gene (amh).

Correction to ‘The onset of ecological diversification 50 years after colonization of a crater lake by haplochromine cichlid fishes’

Proc. R. Soc. B 285 , 20180171. (Published Online 15 August 2018). ([doi:10.1098/rspb.2018.0171][1]) There is an error in the following sentence (first sentence in the … [1]: http://dx.doi.org/10.1098/rspb.2018.0171