Fredrik Haas

An analysis of population genetic differentiation and genotype-phenotype association across the hybrid zone of carrion and hooded crows using microsatellites and MC1R.

The all black carrion crow (Corvus corone corone) and the grey and black hooded crow (Corvus corone cornix) meet in a narrow hybrid zone across Europe. To evaluate the degree of genetic differentiation over the hybrid zone, we genotyped crows from the centre and edges of the zone, and from allopatric populations in northern (Scotland–Denmark–Sweden) and southern Europe (western–central northern Italy), at 18 microsatellites and at a plumage candidate gene, the MC1R gene. Allopatric and edge populations were significantly differentiated on microsatellites, and populations were isolated by distance over the hybrid zone in Italy. Single‐locus analyses showed that one locus, CmeH9, differentiated populations on different sides of the zone at the same time as showing only weak separation of populations on the same side of the zone. Within the hybrid zone there was no differentiation of phenotypes at CmeH9 or at the set of microsatellites, no excess of heterozygotes among hybrids and low levels of linkage disequilibrium between markers. We did not detect any association between phenotypes and nucleotide variation at MC1R, and the two most common haplotypes occurred in very similar frequencies in carrion and hooded crows. That we found a similar degree of genetic differentiation between allopatric and edge populations irrespectively of their location in relation to the hybrid zone, no differentiation between phenotypes within the hybrid zone, and neither heterozygote excess nor consistent linkage disequilibrium in the hybrid zone, is striking considering that carrion and hooded crows are phenotypically distinct and sometimes recognised as separate species.

Hybrid speciation through sorting of parental incompatibilities in Italian sparrows

Speciation by hybridization is emerging as a significant contributor to biological diversification. Yet, little is known about the relative contributions of (i) evolutionary novelty and (ii) sorting of pre‐existing parental incompatibilities to the build‐up of reproductive isolation under this mode of speciation. Few studies have addressed empirically whether hybrid animal taxa are intrinsically isolated from their parents, and no study has so far investigated by which of the two aforementioned routes intrinsic barriers evolve. Here, we show that sorting of pre‐existing parental incompatibilities contributes to intrinsic isolation of a hybrid animal taxon. Using a genomic cline framework, we demonstrate that the sex‐linked and mitonuclear incompatibilities isolating the homoploid hybrid Italian sparrow at its two geographically separated hybrid–parent boundaries represent a subset of those contributing to reproductive isolation between its parent species, house and Spanish sparrows. Should such a sorting mechanism prove to be pervasive, the circumstances promoting homoploid hybrid speciation may be broader than currently thought, and indeed, there may be many cryptic hybrid taxa separated from their parent species by sorted, inherited incompatibilities.

Hybrid zone maintenance by non-adaptive mate choice

In a spatial simulation we show that formation of a stable, narrow hybrid zone requires no selection, only that individuals can recognize their own population type since this is a prerequisite for assortative mating. The European crow occurs in two species/subspecies that meet in a long hybrid zone, the black carrion crow Corvus corone and the grey and black hooded crow C. cornix. In a previous study (Brodin A, Haas F (2006) Anim Behav 72:139) we mimicked sexual imprinting in nestling crows with artificial neural networks, using a learning process that simulates proximate retina perception. The networks were trained on 700 images to recognize either carrion, hooded or hybrid phenotypes as their own. After training the networks were exposed to 300 new, unfamiliar pictures of crows. The networks that had been trained on pure subspecies then showed strong preference for their own type. Networks trained on hybrid crows showed weaker preference for their own type. Assuming that these preferences will determine mate choice preferences we have combined them with empirical data on dispersal of young crows to investigate what kind of geographical distribution pattern this would create. We then assume that the two subspecies meet and hybridize along a straight border. In only 60 generations a stable, narrow hybrid zone that resembles the real hybrid zone was formed. This zone remained stable over time. With minor adjustments of parameters the results would not only fit the width but also the shapes of the clines in the field.

Morphology-function relationships and repeatability in the sperm of Passer sparrows

Sperm performance is likely to be an important determinant of male reproductive success, especially when females copulate with multiple males. Understanding sperm performance is therefore crucial to fully understand the evolution of male reproductive strategies. In this study, we examined the repeatability of sperm morphology and motility measures over three breeding seasons, and we studied relationships between sperm morphology and function. We conducted this study in wild‐derived captive house sparrows (Passer domesticus) and Spanish sparrows (P. hispaniolensis). Results for the two species were similar. As predicted from results in other passerine species, total sperm length was highly repeatable across ejaculates, and repeatability for the length of other components was moderate. The repeatability of sperm swimming speed across ejaculates was lower, but statistically significant, suggesting that sperm velocity may be a relatively dynamic trait. Surprisingly, swimming speed did not correlate with the relative length of the midpiece, and it correlated negatively with the relative length of the flagellum and with total sperm length. This pattern is the opposite of what theory predicts and differs from what has been found in house sparrows before. Also contrary to previous work, we found no evidence that total sperm length correlates with sperm longevity. These results therefore highlight the need for a better understanding of relationships between sperm morphology and function in passerine birds. J. Morphol. 276:370–377, 2015.

Testing a post-copulatory pre-zygotic reproductive barrier in a passerine species pair

Sexual selection may drive speciation, but most research focuses on pre-copulatory sexual selection, overlooking post-copulatory processes. Post-copulatory sexual selection in allopatric populations could drive divergence in post-copulatory pre-zygotic (PCPZ) phenotypes, limiting gene flow upon secondary contact. Here, we performed in vitro experiments examining one potential PCPZ barrier between two closely related passerine species, house sparrows (Passer domesticus) and Spanish sparrows (Passer hispaniolensis). In birds, crossing in the vagina may be particularly challenging for sperm, so we tested the effect of female reproductive tract fluids on sperm swimming speed and motility. If a PCPZ barrier exists at this stage of the fertilization process, heterospecific female fluids are predicted to reduce sperm swimming speed or motility relative to conspecific female fluid. We found that house sparrow female fluids affected the two species’ sperm asymmetrically, depending on the control sperm velocity and male species. Overall, however, sperm performed equally in conspecific and heterospecific female fluids, and the species had similar sperm morphology and sperm swimming performance. Low divergence in PCPZ phenotypes between species, perhaps because post-copulatory sexual selection is stabilizing or only moderately strong in these taxa, may be insufficient to cause an overall PCPZ barrier. Reinforcement may be unlikely to drive PCPZ barriers for this species pair, because relatively effective pre-copulatory barriers exist between the species, and because hybrids can be quite successful. Testing the role of PCPZ barriers in birds with more divergent PCPZ phenotypes will improve our understanding of speciation in passerines.

Identification of 20 polymorphic microsatellite loci in European crow (Corvus corone) from existing passerine loci

The European crow (Corvus corone) occurs in two subspecies (or species) with distinct plumage coloration: the black carrion crow (C. c. corone) and the grey and black hooded crow (C. c. cornix). We tested 42 passerine microsatellite loci for amplification in the European crow and identified 20 loci that were both polymorphic and easy to score. In 50 individuals sampled in the Danish part of the species’ pan‐European hybrid zone, the number of alleles ranged between two and 21. One locus deviated from Hardy–Weinberg equilibrium and had a high estimated null allele frequency. These 20 loci were highly successful in amplifying polymorphic products also in other crow populations and in another Corvidae species, the rook (Corvus frugilegus).

Effect of Species Interaction on Beak Integration in an Avian Hybrid Species Complex

Theory predicts that variability in size and the shape of a morphological trait should often be stable both at the intra- and interspecific level. We studied variation in beak integration among several populations of two species of the genus Passer, a hybrid species, the Italian sparrow (Passer italiae) and one of its parents, the Spanish sparrow (Passer hispaniolensis). We show that the general shape of the beak has been conserved in these two species and that hybrid speciation has had no major effects on beak integration. However, in young, sympatric populations, phenotypic integration between beak height and length decreased significantly, to the extent that these two dimensions apparently became independent. This displacement in phenotypic integration seems to be accompanied with changes in the distribution of phenotypic variation at the univariate level. This suggests that while beak shape may have been constrained over evolutionary time-scales and major hybridization events (i.e. the formation of the hybrid Italian sparrow), under specific selection regimes linked to secondary contact, it can evolve rapidly.

Experimental evidence for ovarian hypofunction in sparrow hybrids

BackgroundPostzygotic isolation in the form of reduced viability and/or fertility of hybrids may help maintain species boundaries in the face of interspecific gene flow. Past hybridization events between house sparrows (Passer domesticus) and Spanish sparrows (P. hispaniolensis) have given rise to a homoploid hybrid species, the Italian sparrow (P. italiae). Although genetic incompatibilities are known to isolate these three species, the biological consequences of these incompatibilities are still unknown in early generation hybrids.MethodsWe investigated whether F1 hybrids between house and Spanish sparrows experience reduced viability or fertility. More specifically, we generated hybrids through controlled crosses in aviaries, and compared ovaries of female hybrids with female of pure-species sparrows.ResultsWe found that overall, hybrid ovaries were underdeveloped and that half of all female hybrids exhibited symptoms of ovarian hypofunction (ovarian atrophy and complete absence of developed follicles).ConclusionsFertility in hybrids is a common consequence or post-zygotic barriers between species. We discuss these results in light of previous findings on genetic incompatibilities between the parent species and the potential role of incompatibilities in hybrid speciation, a rare evolutionary process in birds.