Transgressive segregation in mating traits drives hybrid speciation.

Hybridization can rapidly generate novel genetic variation, which can promote ecological speciation by creating novel adaptive phenotypes. However, it remains unclear how hybridization, creating novel mating phenotypes (e.g., mating season, genitalia shapes, sexual displays, mate preferences), affects speciation especially when the phenotypes do not confer adaptive advantages. Here, based on individual-based evolutionary simulations, we propose that transgressive segregation of mating traits can drive incipient hybrid speciation. Simulations demonstrated that incipient hybrid speciation occurred most frequently when the hybrid population received moderate continued immigration from parental lineages causing recurrent episodes of hybridization. Recurrent hybridization constantly generated genetic variation, which promoted the rapid stochastic evolution of mating phenotypes in a hybrid population. The stochastic evolution continued until a novel mating phenotype came to dominate the hybrid population, which reproductively isolates the hybrid population from parental lineages. However, too frequent hybridization rather hindered the evolution of reproductive isolation by inflating the variation of mating phenotypes to produce phenotypes allowing mating with parental lineages. Simulations also revealed conditions for long-term persistence of hybrid species after their incipient emergence. Our results suggest that recurrent transgressive segregation of mating phenotypes can offer a plausible explanation for hybrid speciation and radiations that involved little adaptive ecological divergence

An introgressed wing pattern acts as a mating cue.

Heliconius butterflies provide good examples of both homoploid hybrid speciation and ecological speciation. In particular, examples of adaptive introgression have been detected among the subspecies of Heliconius timareta, which acquired red color pattern elements from H. melpomene. We tested whether the introgression of red wing pattern elements into H. timareta florencia might also be associated with incipient reproductive isolation (RI) from its close relative, H. timareta subsp. nov., found in the eastern Andes. No choice experiments show a 50% reduction in mating between females of H. t. subsp. nov. and males of H .t. florencia, but not in the reciprocal direction. In choice experiments using wing models, males of H. timareta subsp. nov. approach and court red phenotypes less than their own, whereas males of H. t. florencia prefer models with a red phenotype. Intrinsic postzygotic isolation was not detected in crosses between these H. timareta races. These results suggest that a color pattern trait gained by introgression is triggering RI between H. timareta subsp. nov. and H. t. florencia.We thank Universidad del Rosario for awarding Mauricio Linares the project FIUR, DVG-122, which funded part of the fieldwork and the maintenances of insectary cages at La Vega, Cundinamarca. We also thank Facultad de Ciencias at Universidad de los Andes for awarding APS and ML a “Proyecto Semilla,” and private donations to the latter, toward the funding of part of this project. We also thank the Autoridad Nacional de Licencias Ambientales of Colombia (ANLA) for the collecting permit number 161. Dr. Nicola Clerici provided help with the production of Figure 1.This is the author accepted manuscript. The final version is available from Wiley via http://dx.doi.org/10.1111/evo.1267

Strong selection on male plumage in a hybrid zone between a hybrid bird species and one of its parents

Homoploid hybrid speciation (HHS) requires reproductive barriers between hybrid and parent species, despite incomplete reproductive isolation (RI) between the parents. Novel secondary sexual trait values in hybrids may cause prezygotic isolation from both parents, whereas signals inherited by the hybrid from one parent species may cause prezygotic isolation with the other. Here we investigate whether differences in male plumage function as a premating barrier between the hybrid Italian sparrow and one of its parent species, the house sparrow, in a narrow Alpine hybrid zone. Italian sparrow male plumage is a composite mosaic of the parental traits, with its head plumage most similar to its other parent, the Spanish sparrow. We use geographical cline analysis to examine selection on three plumage traits, 75 nuclear single nucleotide polymorphisms (SNPs) and hybrid indices based on these SNPs. Several SNPs showed evidence of restricted introgression in the Alps, supporting earlier findings. Crown colour exhibited the narrowest plumage cline, representing a 37% (range 4–65%) drop in fitness. The cline was too narrow to be due to neutral introgression. Only crown colour was significantly bimodal in the hybrid zone. Bimodality may be due to RI or a major QTL, although fitness estimates suggest that selection contributes to the pattern. We discuss the implications with respect to HHS and the species status of the Italian sparrow

Evolutionary pathways driven by female mate choice : the curious case of the squalius alburnoides allopolyploid fish complex

Tese de doutoramento, Biologia (Etologia), Universidade de Lisboa, Faculdade de Ciências, 2018Many asexual animals are sexual parasites that reproduce with sympatric species, leading to genetic, ecological and behavioural challenges. Several mechanisms allow the coexistence of sexuals and asexuals, and, over time, the latter may regain sexual reproduction and develop an independent reproductive dynamics, paving the way to the arising of new species through hybrid speciation. Mate choice may play a relevant role in all evolutionary stages of asexual organisms, either contributing to their persistence in hybrid state or routing them towards hybrid speciation. Here, we studied mate choice in the allopolyploid cyprinid Squalius alburnoides, namely its role in driving the evolutionary pathways of this hybrid complex. Bridging together genetic, theoretical and experimental approaches, we aimed at assessing: a) the role of mate choice in driving population stability or routing populations towards hybrid speciation; b) the influence of egg allocation, fertilization rate and offspring survival in shaping the reproductive dynamics and genomotype composition of populations; and c) the gameplay between mate choice by hybrid females and genetic introgression and variability. In the one hand, mate choice by hybrid females seems able to uphold the persistence of populations in their hybrid state by maintaining the reproductive dynamics between the interdependent genomotypes and sympatric congeneric species, and also by guaranteeing the maintenance of high genetic variability. On the other hand, when particular conditions are met, mate choice by hybrid females may also route populations towards hybrid speciation, namely via tetraploidization. The findings reported herein also include the first ever described case of naturally occurring androgenesis in vertebrates. In a general perspective, Squalius alburnoides’ hard-to-combine features challenge even the most conservative views about the role of hybridization in species’ diversification. Studying this allopolyploid complex is like looking at a snapshot of evolution and, undoubtedly, a privilege to every passionate evolutionary biologist

Hybridization promotes color polymorphism in the aposematic harlequin poison frog, Oophaga histrionica

Whether hybridization can be a mechanism that drives phenotypic diversity is a widely debated topic in evolutionary biology. In poison frogs (Dendrobatidae), assortative mating has been invoked to explain how new color morphs persist despite the expected homogenizing effects of natural selection. Here, we tested the complementary hypothesis that new morphs arise through hybridization between different color morphs. Specifically, we (1) reconstructed the phylogenetic relationships among the studied populations of a dart-poison frog to provide an evolutionary framework, (2) tested whether microsatellite allele frequencies of one putative hybrid population of the polymorphic frog O. histrionica are intermediate between O. histrionica and O. lehmanni, and (3) conducted mate-choice experiments to test whether putatively intermediate females prefer homotypic males over males from the other two populations. Our findings are compatible with a hybrid origin for the new morph and emphasize the possibility of hybridization as a mechanism generating variation in polymorphic species. Moreover, because coloration in poison frogs is aposematic and should be heavily constrained, our findings suggest that hybridization can produce phenotypic novelty even in systems where phenotypes are subject to strong stabilizing selection

Demographic modeling 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 modeling 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

Phylogenetics, Population Genetics, and Evolution of the Mallard Complex

Speciation is primarily regarded as an ancestral split that results in two distinct taxonomic units, and proceeds in stages along a continuum from initiation (i.e., population divergence) to completion (i.e., reproductively isolated species). Establishing how and why populations diverge, including the primary mechanisms influencing these events is a major objective for evolutionary scientists. Focusing on incipient forms, researchers attempt to disentangle the antagonistic nature of selection, genetic drift, and gene flow in the speciation process. In chapter 1, I investigate the phylogenetic relationships of 14 closely related taxa within the mallard complex (Anas spp.) that underwent a radiation within the past one million years. Using mitochondrial DNA (mtDNA) and 20 nuclear loci for one to five individuals per taxon, I further examine how recombination and hybridization affect species tree reconstructions. In general, relationships within major clades were robust to treatment of recombination (i.e., ignoring or filtering) and inclusion or exclusion of hybridizing taxa, but branch lengths and posterior support were sensitive to both treatments. Of the 14 taxa, the most confounded relationships were those within the New World (NW) group comprising the sexually dichromatic mallard (Anas platyrhynchos) and the monochromatic American black duck (A. rubripes; black duck ), mottled duck (A. fulvigula), and Mexican duck (A. [p.] diazi). Finally, I address discordance between nuclear, morphometric, and mitochondrial trees, particularly with regard to the placement of the Hawaiian duck (A. wyvilliana), Philippine duck (A. luzonica), and two spot-billed ducks (A. zonorhyncha and A. poecilorhyncha) and discuss how alternative modes of speciation (i.e., hybrid speciation) may lead to variance in these relationships. In Chapter 2, I attempt to disentangle the evolutionary relationships of the New World (NW) group using mtDNA and 17 nuclear loci for a larger per taxon sample size (24-25 individuals per taxon). In general, whereas both Florida and Gulf Coast mottled ducks were differentiated from one another and from the other taxa (mean ΦST = 0.024 - 0.064), mallards, American black ducks, and Mexican duck were not significantly differentiated among nuclear markers (mean ΦST \u3c 0.020). Using coalescent methods to estimate rates of gene flow between mallards and each of the monochromatic taxa generally supported hybridization, but I could not reject complete isolation for any pairwise comparison. Furthermore, species tree reconstructions revealed that phylogenetic relationships were sensitive to stochastic sampling of individuals likely due to incomplete lineage sorting or hybridization. I conclude that members of the NW Mallard group appear to be adaptive incipient morphs, and that future work should focus on genomic regions under selection to better understand the stage and process of speciation in this group. In Chapter 3, I use restriction site associated DNA (RAD) sequencing methods to generate a pseudorandom sampling of 3,563 autosomal and 172 sex-linked (Z chromosome) markers scattered across the genome to more rigorously test the mechanism of speciation between Mexican ducks (N = 105 individuals from six Mexican states and two US states) and mallards (N = 17). Specifically, I aim to determine the stage of speciation and whether speciation has been driven by few loci with large effects versus many loci with small effects, plumage associated differentiation, or genetic drift. Marker comparisons between mallards and Mexican ducks revealed strong discordance among autosomal ΦST = 0.014), sex-linked (mean ΦST = 0.091), and mtDNA (ΦST = 0.12) markers. In general, divergence at autosomal loci followed a stepping stone model, with a gradual transition in genotypic frequencies from North to South

Introgressive hybridisation and incipient ecological speciation amongst saltmarsh Aphrodes leafhoppers

Ecological and host adapted races provide evidence that evolutionary divergence and sympatric speciation can occur through divergent natural selection in the face of continued gene flow. Likewise, hybridisation and introgression (interspecific gene flow) are commonly identified in natural populations, between what are described as distinct taxa. These processes have implications for how we define species and the processes necessary for the persistence and initiation of species and speciation, above and below the species level. The main focus of the present study was elucidation of the nature and extent of differentiation, and processes involved in shaping diversity within and between, species of the Aphrodes leafhopper genus, Curtis 1833, particularly from UK saltmarshes. A multidisciplinary approach was taken, combining the use of morphological, behavioural (vibrational mating signals), mitochondrial DNA (cytochrome oxidase subunit I gene sequencing) and multiple genome-wide nuclear marker (amplified fragment length polymorphism) analyses to test hypotheses relating to taxonomy, ecological speciation and hybridisation among Aphrodes leafhoppers. Of primary interest were: 1) identification of Aphrodes inhabiting saltmarshes, and first confirmation that two species (A. makarovi and A. aestuarina) exist there; 2) comparison of divergent ecological lineages of inland and estuarine A. makarovi, showing possible incipient speciation and evidence of convergent morphological evolution of estuarine A. makarovi and A. aestuarina; 3) exploration of the evolutionary significance of an introgressed hybrid population of A. aestuarina, found only in the Medway estuary, showing complete mitochondrial capture and some nuclear introgression.EThOS - Electronic Theses Online ServiceGBUnited Kingdo

Constraints to speciation despite divergence in an old haplochromine cichlid lineage.

Most of the 500+ cichlid species of Lake Victoria evolved very rapidly in the wake of an adaptive radiation within the last 15'000 years. All 500 species have evolved from just one out of five old cichlid lineages that colonized the lake. Endemic to the Lake Victoria region, Astatoreochromis alluaudi is a member of an old haplochromine lineage that never speciated in the region. Even though the species occurs in a wide range of habitats, there were no indications of evolutionary diversification. Here, we tested predictions of several hypothetical mechanisms that might constrain speciation, including high dispersal rates, a generalist life style and the lack of behavioral assortative mating. Genomic analyses of individuals from thirteen populations revealed several genomically distinct groups, associated with major habitat classes, indicating the existence of two distinct ecotypes. We found significant phenotypic differences between these ecotypes in the wild, which were retained under common-garden conditions, potentially indicating heritable phenotypic adaptations. Female mate choice experiments revealed the absence of behavioural assortative mating despite genetic and phenotypic differentiation between ecotypes. We suggest that the lack of coupling between behavioral mating preferences and phenotypic and genetic divergence constrains speciation in this cichlid

Introgressive hybridisation and incipient ecological speciation amongst saltmarsh Aphrodes leafhoppers

Ecological and host adapted races provide evidence that evolutionary divergence and sympatric speciation can occur through divergent natural selection in the face of continued gene flow. Likewise, hybridisation and introgression (interspecific gene flow) are commonly identified in natural populations, between what are described as distinct taxa. These processes have implications for how we define species and the processes necessary for the persistence and initiation of species and speciation, above and below the species level. The main focus of the present study was elucidation of the nature and extent of differentiation, and processes involved in shaping diversity within and between, species of the Aphrodes leafhopper genus, Curtis 1833, particularly from UK saltmarshes. A multidisciplinary approach was taken, combining the use of morphological, behavioural (vibrational mating signals), mitochondrial DNA (cytochrome oxidase subunit I gene sequencing) and multiple genome-wide nuclear marker (amplified fragment length polymorphism) analyses to test hypotheses relating to taxonomy, ecological speciation and hybridisation among Aphrodes leafhoppers. Of primary interest were: 1) identification of Aphrodes inhabiting saltmarshes, and first confirmation that two species (A. makarovi and A. aestuarina) exist there; 2) comparison of divergent ecological lineages of inland and estuarine A. makarovi, showing possible incipient speciation and evidence of convergent morphological evolution of estuarine A. makarovi and A. aestuarina; 3) exploration of the evolutionary significance of an introgressed hybrid population of A. aestuarina, found only in the Medway estuary, showing complete mitochondrial capture and some nuclear introgression