Lars Erik Johannessen

Mate choice and imprinting in birds studied by cross-fostering in the wild

Sexual–selection theories generally assume that mating preferences are heritable traits. However, there is substantial evidence that the rearing environment may be important for the development of mating preferences, indicating that they may be learnt, or modified by experience. The relative importance of such sexual imprinting across species remains largely unexplored. Here, we report results of a large–scale cross–fostering experiment in the wild in which nestling birds were raised by parents of a different species. We show that resulting sexual imprinting may have a negative effect on pairing success in one species (the great tit, Parus major), but not in two other species (the blue tit, P. caeruleus and the pied flycatcher, Ficedula hypoleuca). A remarkable variation thus seems to exist, even between species that are congeneric and have similar breeding ecologies. The cross–fostering resulted in heterospecific pairings between the two tit species (female blue tit breeding with male great tit), which has never, to our knowledge, been previously documented. However, the chicks fledging from these nests were all blue tit.

Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations

Spermatozoa vary greatly in size and shape among species across the animal kingdom. Postcopulatory sexual selection is thought to be the major evolutionary force driving this diversity. In contrast, less is known about how sperm size varies among populations of the same species. Here, we investigate geographic variation in sperm size in barn swallows Hirundo rustica, a socially monogamous passerine with a wide Holarctic breeding distribution. We included samples from seven populations and three subspecies: five populations of ssp. rustica in Europe (Czech, Italy, Norway, Spain, and Ukraine), one population of ssp. transitiva in Israel, and one population of ssp. erythrogaster in Canada. All sperm traits (head length, midpiece length, tail length, and total length) varied significantly among populations. The variation among the European rustica populations was much lower than the differences among subspecies, indicating that sperm traits reflect phylogenetic distance. We also performed a test of the relationship between the coefficient of between-male variation in total sperm length and extrapair paternity levels across different populations within a species. Recent studies have found a strong negative relationship between sperm size variation and extrapair paternity among species. Here, we show a similar negative relationship among six barn swallow populations, which suggests that the variance in male sperm length in a population is shaped by the strength of stabilizing postcopulatory sexual selection.

Imprinted species recognition lasts for life in free-living great tits and blue tits

Species recognition may be learned through imprinting early in life. Imprinting has normally been studied under highly unnatural conditions in the laboratory. We tested whether species recognition mediated through imprinting is individually modifiable in a field setting where great tits, Parus major, have been artificially cross-fostered to blue tits, Cyanistes caeruleus, and vice versa. We have shown previously that cross-fostered birds have deviant species recognition, in terms of both mate choice and aggressive responses towards rivals. Natural interactions among conspecifics and heterospecifics are common in these populations, potentially giving cross-fostered birds scope for relearning their species identity. We tested whether species recognition may change with experience during adulthood by comparing the aggressive response of cross-fostered birds and controls of different ages towards caged intruders. When breeding, cross-fostered birds responded aggressively towards same-sex individuals of their heterospecific foster species, while unmanipulated controls responded mainly towards conspecifics. We found that the aggressive response decreased with age at similar rates in both treatments and in both species. Moreover, there was no effect of age on the relative response towards conspecifics and heterospecifics in either treatment. Hence, we found no evidence that the species recognition behaviour towards same-sex individuals is shifted towards conspecifics with age in interspecifically cross-fostered birds. We conclude that species recognition is irreversible once it has been established in free-living great tits and blue tits. This is the first study to investigate the stability of species recognition in the field.

The evolutionary history of Afrocanarian blue tits inferred from genomewide SNPs

A common challenge in phylogenetic reconstruction is to find enough suitable genomic markers to reliably trace splitting events with short internodes. Here, we present phylogenetic analyses based on genomewide single‐nucleotide polymorphisms (SNPs) of an enigmatic avian radiation, the subspecies complex of Afrocanarian blue tits (Cyanistes teneriffae). The two sister species, the Eurasian blue tit (Cyanistes caeruleus) and the azure tit (Cyanistes cyanus), constituted the out‐group. We generated a large data set of SNPs for analysis of population structure and phylogeny. We also adapted our protocol to utilize degraded DNA from old museum skins from Libya. We found strong population structuring that largely confirmed subspecies monophyly and constructed a coalescent‐based phylogeny with full support at all major nodes. The results are consistent with a recent hypothesis that La Palma and Libya are relic populations of an ancient Afrocanarian blue tit, although a small data set for Libya could not resolve its position relative to La Palma. The birds on the eastern islands of Fuerteventura and Lanzarote are similar to those in Morocco. Together they constitute the sister group to the clade containing the other Canary Islands (except La Palma), in which El Hierro is sister to the three central islands. Hence, extant Canary Islands populations seem to originate from multiple independent colonization events. We also found population divergences in a key reproductive trait, viz. sperm length, which may constitute reproductive barriers between certain populations. We recommend a taxonomic revision of this polytypic species, where several subspecies should qualify for species rank.

Reproductive strategy and singing activity: blue tit and great tit compared

The costs and benefits of bird song are likely to vary among species, and different singing patterns may reflect differences in reproductive strategies. We compared temporal patterns of singing activity in two songbird species, the blue tit (Cyanistes caeruleus) and the great tit (Parus major). The two species live side by side year round, and they have similar breeding ecology and similar rates of extra-pair paternity. However, they differ in two aspects of reproductive strategy that may have an influence on song output: blue tits are facultatively polygynous and have a fairly short breeding season with almost no second broods, whereas great tits are socially monogamous but more commonly raise second broods. We found that great tit males continued singing at high levels during the egg-laying and incubation periods, while monogamously paired blue tit males strongly reduced singing activity after the first days of egg-laying by their female. Since males of both species sang much more intensely shortly before sunrise than after sunrise, at midday or in the evening, this difference was most conspicuous at dawn. No differences in singing activity were found within species when testing for male age. We suggest that in contrast to blue tits, great tit males continued singing after egg-laying to defend the territory and to encourage the female for a possible second brood.

Vertical and horizontal transmission of nest site preferences in titmice

Social learning is widely used among vertebrates to acquire information about a variable environment. We conducted a study of social learning in the wild which involved cross-fostering eggs of blue tits, Cyanistes caeruleus, to nests of great tits, Parus major, and vice versa. This allowed us to quantify the consequences of being reared in a different social context but in an environment otherwise natural to the birds. We studied choice of nest site by offering to the local recruits either a small or a large nestbox. Most blue tits bred in small nestboxes, whereas most great tits used the large boxes. Size of the natal nestbox affected subsequent box choice. In addition, in blue tits, more cross-fostered birds than controls nested in large nestboxes, with an opposite result for cross-fostered great tits. Apparently, as a consequence of sexual misimprinting on their foster parents, the cross-fostered young used members of the foster species as models for subsequent nest site choice. Such social copying may apply broadly to other types of behaviours and not only to the choice of nest site. This study demonstrates both vertical and horizontal transmission of nest site preference of two vertebrates in the wild. Future studies should try to find out how animals balance the use of personal experience with the information socially acquired.

Interspecific cross-fostering affects mate guarding behaviour in great tits (Parus major)

Mate guarding is thought to decrease the likelihood of cuckoldry and, hence, increase the fitness of guarding males. Mate guarding is costly for males and must be traded off with other fitness-enhancing behaviours. Over several years, we have cross-fostered great tits ( Parus major ) to blue tits ( Cyanistes caeruleus ) and this experimental treatment has influenced the mate and rival recognition of cross-fostered birds. Here we show that cross-fostered great tit males mate guard their females less than do control great tits, regardless of whether the cross-fostered males were mated to great tit females or cross-fostered blue tit females. Cross-fostered great tit males sang more and interacted more frequently with blue tit males than did controls. Females paired to males of the two groups did not differ in the extent to which they initiated movements away from their mates. We conclude that the altered species-assortative behaviour resulting from interspecific cross-fostering influences mate guarding in great tit males, probably by cross-fostered males increasing investment in territorial behaviour at the expense of mate guarding, and/or by cross-fostered males mate guarding less due to a reduced affinity for their female. Such trade-offs may have a general significance for mate guarding species.

No cultural transmission of species recognition between parents and offspring in free-living great tits and blue tits

Imprinting plays a key role in the development of species recognition, with young imprinting upon the morphological characters of their parents. However, the potential role that cultural transmission might play in species recognition remains largely uninvestigated. Great tits (Parus major) and blue tits (Cyanistes caeruleus) do not normally perceive each other as sexual competitors or potential partners. However, after reciprocal interspecific cross-fostering, both species may perceive individuals of the foster species as potential rivals or mates. Although the experience of being raised by heterospecifics clearly has affected the species recognition of cross-fostered birds, some of them breed naturally with conspecifics. The offspring of such cross-fostered birds (OCF) are hence raised by parents that look like ordinary conspecifics but display deviant species recognition as compared to controls in terms of aggressive response towards rivals. Comparing the aggressive behavior of OCF, cross-fostered birds and controls towards territorial intruders may thus help tease apart the influence of morphological vs behavioral cues of parents in the development of offspring species recognition. To this end, we compared birds from all three treatments with respect to their aggressive response to territorial intruders of both species during the breeding season. OCF and controls did not differ in their pattern of response towards heterospecific and conspecific stimuli. Compared to cross-fostered birds, OCF and controls showed less aggression towards heterospecific intruders, while the response towards conspecific intruders did not differ between treatments. These results demonstrate that both tit species imprint on the morphological characters of their parents, but that parental behavior is not important for the development of species recognition in terms of aggressive response towards territorial intruders.

Sperm performance in conspecific and heterospecific female fluid

Abstract Divergent sexual selection within allopatric populations may result in divergent sexual phenotypes, which can act as reproductive barriers between populations upon secondary contact. This hypothesis has been most tested on traits involved in precopulatory sexual selection, with less work focusing on traits that act after copulation and before fertilization (i.e., postcopulatory prezygotic traits), particularly in internally fertilizing vertebrates. However, postcopulatory sexual selection within species can also drive trait divergence, resulting in reduced performance of heterospecific sperm within the female reproductive tract. Such incompatibilities, arising as a by‐product of divergent postcopulatory sexual selection in allopatry, can represent reproductive barriers, analogous to species‐assortative mating preferences. Here, we tested for postcopulatory prezygotic reproductive barriers between three pairs of taxa with diverged sperm phenotypes and moderate‐to‐high opportunity for postcopulatory sexual selection (barn swallows Hirundo rustica versus sand martins Riparia riparia, two subspecies of bluethroats, Luscinia svecica svecica versus L. s. namnetum, and great tits Parus major versus blue tits Cyanistes caeruleus). We tested sperm swimming performance in fluid from the outer reproductive tract of females, because the greatest reduction in sperm number in birds occurs as sperm swim across the vagina. Contrary to our expectations, sperm swam equally well in fluid from conspecific and heterospecific females, suggesting that postcopulatory prezygotic barriers do not act between these taxon pairs, at this stage between copulation and fertilization. We therefore suggest that divergence in sperm phenotypes in allopatry is insufficient to cause widespread postcopulatory prezygotic barriers in the form of impaired sperm swimming performance in passerine birds.

Reduced genetic diversity and sperm motility in the endangered Gran Canaria Blue Chaffinch Fringilla teydea polatzeki

AbstractThe Blue Chaffinch (Fringilla teydea) is endemic to the Canary Islands and restricted to the pine forests on Tenerife (ssp. teydea) and Gran Canaria (ssp. polatzeki). While the teydea population is large and stable, the polatzeki population underwent a dramatic decline in the twentieth century and currently numbers less than 200 individuals. Here, we show that microsatellite allelic diversity is lower in polatzeki than in teydea, consistent with a genetic bottleneck scenario. Our genotyped polatzeki individuals, which were wild-caught but currently used in a captive breeding programme, have the same allelic diversity as free-ranging birds. However, the captive polatzeki males seem to have reduced sperm motility as compared with captive teydea males, which could be an effect of reduced genetic diversity. Because polatzeki and teydea are phylogenetically distinct, they should be recognized as Evolutionarily Significant Units by conservation authorities. We also recommend maintaining the captive polatzeki population as a pre-emptive measure against extinction in the wild.ZusammenfassungEingeschränkte genetische Vielfalt und Spermienbeweglichkeit beim vom Aussterben bedrohten Teide-Blaufinken (Fringilla teydea polatzeki) auf Gran Canaria Der Teide-Blaufink (Fringilla teydea polatzeki) ist auf den Kanarischen Inseln endemisch und lebt ausschließlich in den Pinienwäldern auf Teneriffa (ssp. teydea) und Gran Canaria (ssp. polatzeki). Während die Population auf Teneriffa groß und stabil ist, erfuhr die Population auf Gran Canaria im 20. Jahrhundert einen dramatischen Rückgang und umfasst zur Zeit weniger als 200 Individuen. In dieser Arbeit zeigen wir, dass die allelische Vielfalt der Mikrosatelliten bei Polatzeki geringer als bei Teydea ist, was im Einklang mit einem genetischen „Engpass-Szenario“steht. Unsere genotypisch eindeutig identifizierten Polatzeki-Individuen, die Wildfänge waren und jetzt in Gefangenschaft in einem Brutprogramm eingesetzt werden, zeigten die gleiche allelische Vielfalt wie die Tiere im Freiland. Aber die gefangenen Polatzeki-Männchen scheinen gegenüber den Teydea-Männchen eine reduzierte Spermienbeweglichkeit zu haben, was an einer geringeren genetischen Vielfalt liegen könnte. Weil Polatzeki und Teydea phylogenetisch unterschiedlich sind, sollten sie vom Naturschutz offiziell als Evolutionary Significant Units (ESU) anerkannt werden. Wir empfehlen außerdem, die derzeit in Gefangenschaft gehaltene Polatzeki-Population weiterzuführen als Vorsichtsmaßnahme gegen die mögliche Ausrottung im Freiland.