A Combinatorial View on Speciation and Adaptive Radiation.

Speciation is often thought of as a slow process due to the waiting times for mutations that cause incompatibilities, and permit ecological differentiation or assortative mating. Cases of rapid speciation and particularly cases of rapid adaptive radiation into multiple sympatric species have remained somewhat mysterious. We review recent findings from speciation genomics that reveal an emerging commonality among such cases: reassembly of old genetic variation into new combinations facilitating rapid speciation and adaptive radiation. The polymorphisms in old variants frequently originated from hybridization at some point in the past. We discuss why old variants are particularly good fuel for rapid speciation, and hypothesize that variation in access to such old variants might contribute to the large variation in speciation rates observed in nature

Eukaryote hybrid genomes.

Interspecific hybridization is the process where closely related species mate and produce offspring with admixed genomes. The genomic revolution has shown that hybridization is common, and that it may represent an important source of novel variation. Although most interspecific hybrids are sterile or less fit than their parents, some may survive and reproduce, enabling the transfer of adaptive variants across the species boundary, and even result in the formation of novel evolutionary lineages. There are two main variants of hybrid species genomes: allopolyploid, which have one full chromosome set from each parent species, and homoploid, which are a mosaic of the parent species genomes with no increase in chromosome number. The establishment of hybrid species requires the development of reproductive isolation against parental species. Allopolyploid species often have strong intrinsic reproductive barriers due to differences in chromosome number, and homoploid hybrids can become reproductively isolated from the parent species through assortment of genetic incompatibilities. However, both types of hybrids can become further reproductively isolated, gaining extrinsic isolation barriers, by exploiting novel ecological niches, relative to their parents. Hybrids represent the merging of divergent genomes and thus face problems arising from incompatible combinations of genes. Thus hybrid genomes are highly dynamic and undergo rapid evolutionary change, including genome stabilization in which selection against incompatible combinations results in fixation of compatible ancestry block combinations within the hybrid species. The potential for rapid adaptation or speciation makes hybrid genomes a particularly exciting subject of in evolutionary biology. Here we summarize how introgressed alleles or hybrid species can establish and how the resulting hybrid genomes evolve

Rapid generation of ecologically relevant behavioral novelty in experimental cichlid hybrids.

The East African cichlid radiations are characterized by repeated and rapid diversification into many distinct species with different ecological specializations and by a history of hybridization events between nonsister species. Such hybridization might provide important fuel for adaptive radiation. Interspecific hybrids can have extreme trait values or novel trait combinations and such transgressive phenotypes may allow some hybrids to explore ecological niches neither of the parental species could tap into. Here, we investigate the potential of second-generation (F2) hybrids between two generalist cichlid species from Lake Malawi to exploit a resource neither parental species is specialized on: feeding by sifting sand. Some of the F2 hybrids phenotypically resembled fish of species that are specialized on sand sifting. We combined experimental behavioral and morphometric approaches to test whether the F2 hybrids are transgressive in both morphology and behavior related to sand sifting. We then performed a quantitative trait loci (QTL) analysis using RADseq markers to investigate the genetic architecture of morphological and behavioral traits. We show that transgression is present in several morphological traits, that novel trait combinations occur, and we observe transgressive trait values in sand sifting behavior in some of the F2 hybrids. Moreover, we find QTLs for morphology and for sand sifting behavior, suggesting the existence of some loci with moderate to large effects. We demonstrate that hybridization has the potential to rapidly generate novel and ecologically relevant phenotypes that may be suited to a niche neither of the parental species occupies. Interspecific hybridization may thereby contribute to the rapid generation of ecological diversity in cichlid radiations

Identification of a novel sex determining chromosome in cichlid fishes that acts as XY or ZW in different lineages.

Funder: The Branco Weiss Fellowship – Society in Science; doi: http://dx.doi.org/10.13039/501100001710UNLABELLED: Sex determination systems are highly conserved among most vertebrates with genetic sex determination, but can be variable and evolve rapidly in some. Here, we study sex determination in a clade with exceptionally high sex chromosome turnover rates. We identify the sex determining chromosomes in three interspecific crosses of haplochromine cichlid fishes from Lakes Victoria and Malawi. We find evidence for different sex determiners in each cross. In the Malawi cross and one Victoria cross the same chromosome is sex-linked but while females are the heterogametic sex in the Malawi species, males are the heterogametic sex in the Victoria species. This chromosome has not previously been reported to be sex determining in cichlids, increasing the number of different chromosomes shown to be sex determining in cichlids to 12. All Lake Victoria species of our crosses are less than 15,000 years divergent, and we identified different sex determiners among them. Our study provides further evidence for the diversity and evolutionary flexibility of sex determination in cichlids, factors which might contribute to their rapid adaptive radiations. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s10750-021-04560-7

Altitude and life-history shape the evolution of Heliconius wings.

Phenotypic divergence between closely related species has long interested biologists. Taxa that inhabit a range of environments and have diverse natural histories can help understand how selection drives phenotypic divergence. In butterflies, wing color patterns have been extensively studied but diversity in wing shape and size is less well understood. Here, we assess the relative importance of phylogenetic relatedness, natural history, and habitat on shaping wing morphology in a large dataset of over 3500 individuals, representing 13 Heliconius species from across the Neotropics. We find that both larval and adult behavioral ecology correlate with patterns of wing sexual dimorphism and adult size. Species with solitary larvae have larger adult males, in contrast to gregarious Heliconius species, and indeed most Lepidoptera, where females are larger. Species in the pupal-mating clade are smaller than those in the adult-mating clade. Interestingly, we find that high-altitude species tend to have rounder wings and, in one of the two major Heliconius clades, are also bigger than their lowland relatives. Furthermore, within two widespread species, we find that high-altitude populations also have rounder wings. Thus, we reveal novel adaptive wing morphological divergence among Heliconius species beyond that imposed by natural selection on aposematic wing coloration

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)

Ancient hybridization fuels rapid cichlid fish adaptive radiations.

Understanding why some evolutionary lineages generate exceptionally high species diversity is an important goal in evolutionary biology. Haplochromine cichlid fishes of Africa's Lake Victoria region encompass >700 diverse species that all evolved in the last 150,000 years. How this 'Lake Victoria Region Superflock' could evolve on such rapid timescales is an enduring question. Here, we demonstrate that hybridization between two divergent lineages facilitated this process by providing genetic variation that subsequently became recombined and sorted into many new species. Notably, the hybridization event generated exceptional allelic variation at an opsin gene known to be involved in adaptation and speciation. More generally, differentiation between new species is accentuated around variants that were fixed differences between the parental lineages, and that now appear in many new combinations in the radiation species. We conclude that hybridization between divergent lineages, when coincident with ecological opportunity, may facilitate rapid and extensive adaptive radiation

Multispecies colour polymorphisms associated with contrasting microhabitats in two Mediterranean wrasse radiations.

Intraspecific colour polymorphisms (CPs) present unique opportunities to study fundamental evolutionary questions, such as the link between ecology and phenotype, mechanisms maintaining genetic diversity and their putative role in speciation. Wrasses are highly diverse in ecology and morphology and harbour a variety of colour-polymorphic species. In the Mediterranean Sea, wrasses of the tribe Labrini evolved two species radiations each harbouring several species with a brown and a green morph. The colour morphs occur in complete sympatry in mosaic habitats with rocky outcrops and Neptune grass patches. Morph-specific differences had not been characterized yet and the evolutionary forces maintaining them remained unknown. With genome-wide data for almost all Labrini species, we show that species with CPs are distributed across the phylogeny, but show evidence of hybridization. This suggests that the colour morphs are either ancient and have been lost repeatedly, that they have evolved repeatedly or have been shared via hybridization. Focusing on two polymorphic species, we find that each colour morph is more common in the microhabitat providing the best colour match and that the morphs exhibit additional behavioural and morphological differences further improving crypsis in their respective microhabitats. We find little evidence for genetic differentiation between the morphs in either species. Therefore, we propose that these colour morphs represent a multi-niche polymorphism as an adaptation to the highly heterogeneous habitat. Our study highlights how colour polymorphism (CP) can be advantageous in mosaic habitats and that Mediterranean wrasses are an ideal system to study trans-species polymorphisms, i.e. polymorphisms maintained across several species, in adaptive radiations

Multispecies colour polymorphisms associated with contrasting microhabitats in two Mediterranean wrasse radiations.

Intraspecific colour polymorphisms (CPs) present unique opportunities to study fundamental evolutionary questions, such as the link between ecology and phenotype, mechanisms maintaining genetic diversity and their putative role in speciation. Wrasses are highly diverse in ecology and morphology and harbour a variety of colour-polymorphic species. In the Mediterranean Sea, wrasses of the tribe Labrini evolved two species radiations each harbouring several species with a brown and a green morph. The colour morphs occur in complete sympatry in mosaic habitats with rocky outcrops and Neptune grass patches. Morph-specific differences had not been characterized yet and the evolutionary forces maintaining them remained unknown. With genome-wide data for almost all Labrini species, we show that species with CPs are distributed across the phylogeny, but show evidence of hybridization. This suggests that the colour morphs are either ancient and have been lost repeatedly, that they have evolved repeatedly or have been shared via hybridization. Focusing on two polymorphic species, we find that each colour morph is more common in the microhabitat providing the best colour match and that the morphs exhibit additional behavioural and morphological differences further improving crypsis in their respective microhabitats. We find little evidence for genetic differentiation between the morphs in either species. Therefore, we propose that these colour morphs represent a multi-niche polymorphism as an adaptation to the highly heterogeneous habitat. Our study highlights how colour polymorphism (CP) can be advantageous in mosaic habitats and that Mediterranean wrasses are an ideal system to study trans-species polymorphisms, i.e. polymorphisms maintained across several species, in adaptive radiations

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