Thor Veen

Hybridization and adaptive mate choice in flycatchers

Hybridization in natural populations is strongly selected against when hybrid offspring have reduced fitness. Here we show that, paradoxically, pairing with another species may offer the best fitness return for an individual, despite reduced fitness of hybrid offspring. Two mechanisms reduce the costs to female collared flycatchers of pairing with male pied flycatchers. A large proportion of young are sired by conspecific male collared flycatchers through extra-pair copulations, and there is a bias in favour of male offspring (which, unlike females, are fertile) within hybrid pairs. In combination with temporal variation in breeding success, these cost-reducing mechanisms yield quantitative predictions about when female collared flycatchers should accept a male pied flycatcher as a mate; empirical data agree with these predictions. Apparent hybridization may thus represent adaptive mate choice under some circumstances.

Natural and sexual selection against hybrid flycatchers

While sexual selection is generally assumed to quickly cause or strengthen prezygotic barriers between sister species, its role in causing postzygotic isolation, through the unattractiveness of intermediate hybrids, is less often examined. Combining 24 years of pedigree data and recently developed species-specific molecular markers from collared (Ficedula albicollis) and pied (Ficedula hypoleuca) flycatchers and their hybrids, we were able to quantify all key components of fitness. To disentangle the relative role of natural and sexual selection acting on F1 hybrid flycatchers, we estimated various fitness components, which when combined represent the total lifetime reproductive success of F1 hybrids, and then compared the different fitness components of F1 hybrids to that of collared flycatchers. Female hybrid flycatchers are sterile, with natural selection being the selective force involved, but male hybrids mainly experienced a reduction in fitness through sexual selection (decreased pairing success and increased rate of being cuckolded). To disentangle the role of sexual selection against male hybrids from a possible effect of genetic incompatibility (on the rate of being cuckolded), we compared male hybrids with pure-bred males expressing intermediate plumage characters. Given that sexual selection against male hybrids is a result of their intermediate plumage, we expect these two groups of males to have a similar fitness reduction. Alternatively, hybrids have reduced fitness owing to genetic incompatibility, in which case their fitness should be lower than that of the intermediate pure-bred males. We conclude that sexual selection against male hybrids accounts for approximately 75% of the reduction in their fitness. We discuss how natural and sexual selection against hybrids may have different implications for speciation and conclude that reinforcement of reproductive barriers may be more likely when there is sexual selection against hybrids.

Experimental evidence for innate predator recognition in the Seychelles warbler

Nest predation is a major determinant of fitness in birds and costly nest defence behaviours have evolved in order to reduce nest predation. Some avian studies have suggested that predator recognition is innate whereas others have stressed the importance of learning. However, none of these studies controlled for the genetic origin of the populations investigated and the effect of unfamiliarity with the predator. Here we determined whether experience with a nest predator is a prerequisite for nest defence by comparing predator recognition responses between two isolated but genetically similar Seychelles warbler (Acrocephalus sechellensis) populations, only one of which had experience of the egg predating Seychelles fody (Foudia sechellarum). Individuals in the predator–free population significantly reduced nest guarding compared to individuals in the population with the predator, which indicates that this behaviour was adjusted to the presence of nest predators. However, recognition responses (measured as both alarm call and attack rates) towards a mounted model of the fody were equally strong in both populations and significantly higher than the responses towards either a mounted familiar non–predator and a mounted, novel, non–predator bird species. Responses did not differ with a warblers age and experience with the egg predator, indicating that predator recognition is innate.

Climate change, breeding date and nestling diet: how temperature differentially affects seasonal changes in pied flycatcher diet depending on habitat variation

1. Climate warming has led to shifts in the seasonal timing of species. These shifts can differ across trophic levels, and as a result, predator phenology can get out of synchrony with prey phenology. This can have major consequences for predators such as population declines owing to low reproductive success. However, such trophic interactions are likely to differ between habitats, resulting in differential susceptibility of populations to increases in spring temperatures. A mismatch between breeding phenology and food abundance might be mitigated by dietary changes, but few studies have investigated this phenomenon. Here, we present data on nestling diets of nine different populations of pied flycatchers Ficedula hypoleuca, across their breeding range. This species has been shown to adjust its breeding phenology to local climate change, but sometimes insufficiently relative to the phenology of their presumed major prey: Lepidoptera larvae. In spring, such larvae have a pronounced peak in oak habitats, but to a much lesser extent in coniferous and other deciduous habitats. 2. We found strong seasonal declines in the proportions of caterpillars in the diet only for oak habitats, and not for the other forest types. The seasonal decline in oak habitats was most strongly observed in warmer years, indicating that potential mismatches were stronger in warmer years. However, in coniferous and other habitats, no such effect of spring temperature was found. 3. Chicks reached somewhat higher weights in broods provided with higher proportions of caterpillars, supporting the notion that caterpillars are an important food source and that the temporal match with the caterpillar peak may represent an important component of reproductive success. 4. We suggest that pied flycatchers breeding in oak habitats have greater need to adjust timing of breeding to rising spring temperatures, because of the strong seasonality in their food. Such between-habitat differences can have important consequences for population dynamics and should be taken into account in studies on phenotypic plasticity and adaptation to climate change.

Mandated data archiving greatly improves access to research data

The data underlying scientific papers should be accessible to researchers both now and in the future, but how best can we ensure that these data are available? Here we examine the effectiveness of four approaches to data archiving: no stated archiving policy, recommending (but not requiring) archiving, and two versions of mandating data deposition at acceptance. We control for differences between data types by trying to obtain data from papers that use a single, widespread population genetic analysis, structure. At one extreme, we found that mandated data archiving policies that require the inclusion of a data availability statement in the manuscript improve the odds of finding the data online almost 1000‐fold compared to having no policy. However, archiving rates at journals with less stringent policies were only very slightly higher than those with no policy at all. We also assessed the effectiveness of asking for data directly from authors and obtained over half of the requested datasets, albeit with ~8 d delay and some disagreement with authors. Given the long‐term benefits of data accessibility to the academic community, we believe that journal‐based mandatory data archiving policies and mandatory data availability statements should be more widely adopted.—Vines, T. H., Andrew, R. L., Bock, D. G., Franklin, M. T., Gilbert, K. J., Kane, N. C., Moore, J‐S., Moyers, B. T., Renaut, S., Rennison, D. J., Veen, T., Yeaman, S. Mandated data archiving greatly improves access to research data. FASEB J. 27, 1304–1308 (2013). www.fasebj.org

Cross-fostering reveals seasonal changes in the relative fitness of two competing species of flycatchers

Spatial and temporal heterogeneity in relative fitness of competing species is a key factor affecting the structure of communities. However, it is not intuitive why species that are ecologically similar should differ in their response to environmental changes. Here we show that two sympatric flycatchers differ in reproductive strategy and in sensitivity to harsh environment. The fitness of collared flycatchers (Ficedula albicollis), which are dominant in interference competition, is more sensitive than the fitness of pied flycatchers (Ficedula hypoleuca) to the seasonal decline in environmental conditions. In order to control for the possibility that this pattern arises solely from differences in microhabitat use (i.e. a local niche differentiation), we performed a partial cross-fostering experiment of young between the two species (i.e. resulting in nests containing young of both species). Our results show that the growth of nestling pied flycatchers is less influenced by the seasonal decline in environmental conditions. We suggest that a life-history trade-off between interference competitive ability and robustness to harsh environment promotes a regional coexistence of the two species.

Does migration of hybrids contribute to post-zygotic isolation in flycatchers?

In the face of hybridization, species integrity can only be maintained through post-zygotic isolating barriers (PIBs). PIBs need not only be intrinsic (i.e. hybrid inviability and sterility caused by developmental incompatibilities), but also can be extrinsic due to the hybrids intermediate phenotype falling between the parental niches. For example, in migratory species, hybrid fitness might be reduced as a result of intermediate migration pathways and reaching suboptimal wintering grounds. Here, we test this idea by comparing the juvenile to adult survival probabilities as well as the wintering grounds of pied flycatchers (Ficedula hypoleuca), collared flycatchers (Ficedula albicollis) and their hybrids using stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) in feathers developed at the wintering site. Our result supports earlier observations of largely segregated wintering grounds of the two parental species. The isotope signature of hybrids clustered with that of pied flycatchers. We argue that this pattern can explain the high annual survival of hybrid flycatchers. Hence, dominant expression of the traits of one of the parental species in hybrids may substantially reduce the ecological costs of hybridization.

Multiple post‐mating barriers to hybridization in field crickets

Mechanisms that prevent different species from interbreeding are fundamental to the maintenance of biodiversity. Barriers to interspecific matings, such as failure to recognize a potential mate, are often relatively easy to identify. Those occurring after mating, such as differences in the how successful sperm are in competition for fertilisations, are cryptic and have the potential to create selection on females to mate multiply as a defence against maladaptive hybridization. Cryptic advantages to conspecific sperm may be very widespread and have been identified based on the observations of higher paternity of conspecifics in several species. However, a relationship between the fate of sperm from two species within the female and paternity has never been demonstrated. We use competitive microsatellite PCR to show that in two hybridising cricket species, Gryllus bimaculatus and G. campestris, sequential cryptic reproductive barriers are present. In competition with heterospecifics, more sperm from conspecific males is stored by females. Additionally, sperm from conspecific males has a higher fertilisation probability. This reveals that conspecific sperm precedence can occur through processes fundamentally under the control of females, providing avenues for females to evolve multiple mating as a defence against hybridization, with the counterintuitive outcome that promiscuity reinforces isolation and may promote speciation.

Premating reproductive barriers between hybridising cricket species differing in their degree of polyandry

Understanding speciation hinges on understanding how reproductive barriers arise between incompletely isolated populations. Despite their crucial role in speciation, prezygotic barriers are relatively poorly understood and hard to predict. We use two closely related cricket species, Gryllus bimaculatus and G. campestris, to experimentally investigate premating barriers during three sequential mate choice steps. Furthermore, we experimentally show a significant difference in polyandry levels between the two species and subsequently test the hypothesis that females of the more polyandrous species, G. bimaculatus, will be less discriminating against heterospecific males and hence hybridise more readily. During close-range mating behaviour experiments, males showed relatively weak species discrimination but females discriminated very strongly. In line with our predictions, this discrimination is asymmetric, with the more polyandrous G. bimaculatus mating heterospecifically and G. campestris females never mating heterospecifically. Our study shows clear differences in the strength of reproductive isolation during the mate choice process depending on sex and species, which may have important consequences for the evolution of reproductive barriers.

Diverse reproductive barriers in hybridising crickets suggests extensive variation in the evolution and maintenance of isolation

Reproductive barriers reduce gene flow between populations and maintain species identities. A diversity of barriers exist, acting before, during and after mating. To understand speciation and coexistence, these barriers need to be quantified and their potential interactions revealed. We use the hybridising field crickets Gryllus bimaculatus and G. campestris as a model to understand the full compliment and relative strength of reproductive barriers. We find that males of both species prefer conspecific females, but the effect is probably too weak to represent a barrier. In contrast, prezygotic barriers caused by females being more attracted to conspecific male song and preferentially mounting and mating with conspecifics are strong and asymmetric. Postzygotic barriers vary in direction; reductions in fecundity and egg viability create selection against hybridisation, but hybrids live longer than pure-bred individuals. Hybrid females show a strong preference for G. bimaculatus songs, which together with a complete lack of hybridisation by G. campestris females, suggests that asymmetric gene flow is likely. For comparison, we review reproductive barriers that have been identified between other Gryllids and conclude that multiple barriers are common. Different species pairs are separated by qualitatively different combinations of barriers, suggesting that reproductive isolation and even the process of speciation itself may vary widely even within closely related groups.