Male territorial vocalizations and responses are decoupled in an avian hybrid zone

A core area of speciation research concerns the coevolution of species-specific signals and the selective sensitivity to such signals. Signals and responses to them should be tuned to each other, to be effective in intraspecific communication. Hybrid zones are ideal to study the presence of such 'behavioural coupling' and the mechanisms governing it, and this has rarely been done. Our study examines acoustic signals of males and their response to them in the context of territorial interactions in a natural hybrid zone between two dove species, Streptopelia vinacea and Streptopelia capicola. Male signals are important in hybrid zone dynamics as they are essential for territory establishment, which is crucial for successful reproduction. We tested whether the response of individual male hybrids is linked to how similar their own signal is to the playback signal. We did not find evidence for behavioural coupling. The combined evidence from the low level of response to hybrid and heterospecific signals outside the hybrid zone and a lack of coupling within the hybrid zone suggests that perceptual learning may explain our results. Learning to respond to locally abundant signals may be the best individual strategy and is likely to contribute to the maintenance of a hybrid zone.     

Behavioral asymmetries in a moving hybrid zone

Three narrow hybrid zones exist between hermit and Townsend'swarblers in the Pacific Northwest. Character transition curvessuggest that these zones are moving and that Townsend's warblershave a selective advantage over hermit warblers. This studycompares year-to-year return rates, male persistence on territories,pairing success, pairing patterns, and territory quality of hermitand Townsend's warblers and their hybrids in the WashingtonCascades hybrid zone. There was no difference in the year-to-yearreturn rate between the parental species. Townsend's males weremore successful in maintaining territories and attracting matesthan hermit males. Among mated pairs there were few hermit malescompared to females, independently supporting the inferiorityof hermit males in competition for territories or female mate choicefor Townsend's-like males. I found no difference in the qualityof hermit and Townsend's territories; however, in poor habitatsTownsend's males were more successful at attracting mates, suggestingfemale preference for Townsend's-like males. In high-qualityhabitats, there was no difference in pairing success betweenthe parental species. The fitness of hybrids relative to parentalsaffects the width and movement of the zone. Hybrids were intermediatein their ability to maintain territories and to attract mates, whichshould increase the width of the zone and accelerate its movement.Fewer hybrid males returned to from one year to the next, andamong mated pairs there were few hybrid females relative tomales, suggesting hybrid inferiority, which should narrow thehybrid zone and slow its movement.     

Basal song rate variation in male red-winged blackbirds: sound and fury signifying nothing?

Male red-winged blackbirds (Agelaius phoeniceus) vary substantiallyin how much they sing. We tested whether song rate reflectedthe male’s quality, the quality of his territory, or hisfrequency of interaction with potential competitors. Song ratedeclined with the seasonal decline in nest initiations, suggestingthat song is used to attract females. However, males with highersong rates did not obtain larger harems. This suggests thatfemales do not use male song rate to assess either male qualityor territory quality. If song rate signals male quality to malerivals, and if territory owners are of higher quality than floaters,then owners' song rates should be higher than those of floaters.However, when we removed territory owners temporarily, the songrate of their floater replacements was similar to that of theoriginal owners. Finally, a male’s song rate was not affectedby how frequently he chased intruders, or by the proximity ornumber of neighbors he had. In short, the only information thatbasal song rate of redwinged blackbirds appears to provide toconspecifics is that the territory is occupied. In simulatedterritory takeover attempts, however, song rate was significantlyhigher than the basal rate. Thus, more may be revealed by thesinger in these situations. [Behav Ecol 1991;2:123-132]     

Lower reproductive success in hybrid fur seal males indicates fitness costs to hybridization

Hybridization among organisms can potentially contribute to the processes of evolution, but this depends on the fitness of hybrids relative to parental species. A small, recently formed population of fur seals on subantarctic Macquarie Island contains a high proportion of hybrids (17-30%) derived from combinations of three parental species: Antarctic, subantarctic and New Zealand fur seals. Mitochondrial control-region data (restriction fragment length polymorphisms) and nine microsatellites were used to determine the species composition of breeding adults, and hybrid male fitness was measured by comparing reproductive success (number of genetically inferred paternities) of hybrid and pure-species territory males over 6 years. No correlations were found between male reproductive success and three genetic measures of outbreeding, but this may be due to a relatively small number of dominant males analysed. Territory males fathered 63% of pups, but hybrid males had lower reproductive success than pure-species males despite having the same ability to hold territories. A greater proportion of females in hybrid male territories conceived extra-territorially than those in territories of pure-species males, and most (70 of 82) mated with conspecifics. This suggests the presence of reproductive isolating mechanisms that promote positive assortative mating and reduce the production of hybrid offspring. Although we found no evidence for male sterility in the population, mechanisms that reduce lifetime reproductive success may act to decrease the frequency of hybrids. Our study has identified a disadvantage of hybridization - reduced reproductive success of hybrid sons - that may be contributing to the persistence of pure lineages at Macquarie Island and the temporal decline in hybridization observed there.     

Bounded hybrid superiority in an avian hybrid zone: effects of mate, diet, and habitat choice

There has been considerable debate in the study of hybrid zones as to whether hybrids may be superior to parental types within the area of contact (bounded hybrid superiority). In birds, naturally occurring hybridization is relatively common, and hybridization within this group always involves mate choice. If hybrids are superior, females choosing heterospecific mates should be expected to show higher fitness under the conditions prevalent in the hybrid zone. Hybrid superiority under these circumstances would reduce reinforcement and thereby help to maintain the hybrid zone. To examine this issue, we studied reproductive performances of hybrids and parental species of gulls (Larus occidentalis and Larus glaucescens) at two colonies within a linear hybrid zone along the west coast of the United States. This hybrid zone contains predominantly gulls of intermediate phenotype. Previous studies indicated that hybrids were superior to one or both parental types, but provided no data on possible mechanisms that underlie this hybrid superiority. Using a hybrid index designed specifically for these species, we identified to phenotype more than 300 individuals associated with nests, including both individual males and females within 73 pairs in the central portion of the hybrid zone and 74 pairs in the northern portion of the hybrid zone. There was little evidence of assortative mating, and what little there was resulted solely because of pairings within intergrades. In the central hybrid zone, females paired with hybrid males produced larger clutches and hatched and fledged more chicks compared with females paired to western gull males. This was a result of heavy predation on eggs in sand habitat, where male western gulls established territories. In contrast, many hybrid males established territories in vegetated cover that was less vulnerable to predation. In the northern part of the hybrid zone, clutch size did not differ among pair categories, however, there were differences in hatching and fledging success, with females paired to hybrid males showing better success compared to females paired to glaucous-winged gull males. Hybrids showed better hatching and fledging success in the north because hybrids are more like western gulls than glaucous-winged gulls in foraging behavior, taking a higher percentage of fish in their diet, which enhances chick growth and survival. This is believed to be the first documentation of bounded hybrid superiority that delineates the mechanisms that underlie hybrid superiority.     

A narrow hybrid zone between the grasshoppers Stenobothrus clavatus and Stenobothrus rubicundus (Orthoptera: Gomphocerinae): female preferences for courtship songs

Two grasshopper species, Stenobothrus rubicundus and Stenobothrus clavatus, were previously shown to hybridize in a narrow contact zone on Mount Tomaros in northern Greece. The species are characterized by complex and completely different courtship songs. In the present study, we investigated female preferences for the courtship songs of S. rubicundus, S. clavatus and hybrids in playback experiments. Playback of the courtship songs revealed assortative preferences in females of the parental species: they significantly more often preferred the songs of conspecific males. Hybrid females showed a lower selectivity than parental females, responding somewhat equally eager to playback of the songs of S. clavatus, S. rubicundus, and natural hybrid song, although less actively to the F₁ hybrid song. The results suggest that hybrid males may lose to males of parental species, whereas hybrid females would even have an advantage over parental females. Comparison of responses of females from allopatric populations and Mount Tomaros to different song types shows no evidence for reinforcement. Asymmetry found in female preferences may have implications for the structure of the hybrid zone. © 2013 The Linnean Society of London     

Behavioral correlations across breeding contexts provide a mechanism for a cost of aggression

Identifying correlations among behaviors is important for understandinghow selection shapes the phenotype. Correlated behaviors canindicate constraints on the evolution of behavioral plasticityor may reflect selection for functional integration among behaviors.Obligate cavity-nesting birds provide an opportunity to examinethese correlations because males must defend limited nest cavitieswhile also competing for mating opportunities and providingparental care. Here, I investigated the role of behavioral correlationsin producing a counterintuitive relationship between nest defenseand reproductive success in western bluebirds (Sialia mexicana)such that males that defended their nests most intensely hadthe lowest reproductive success, measured as the number of withinand extrapair offspring that fledged. By experimentally measuringaggression across contexts, I show that this cost of nest defensewas due to the correlated expression of aggression across thecontexts of nest defense and male–male competition coupledwith a trade-off between male–male aggression and parentalcare. In particular, more aggressive males provisioned theirfemales less during incubation and this led to disrupted incubationpatterns and fewer fledged offspring. However, aggressive malesdid not benefit from avoiding parental investment by gainingextrapair fertilizations, and thus, it is unclear how high levelsof aggression are maintained in this population despite apparentcosts. These results suggest that there are constraints to theevolution of plasticity in aggression and emphasize the importanceof considering the integrated behavioral phenotype to understandhow variation in behavior is linked to fitness.     

The rally call recognition in males of two hybridizing partridge species, red-legged (Alectoris rufa) and rock (A. graeca) partridges

The red-legged (Alectoris rufa) and rock (A. graeca) partridges hybridize and produce fertile offspring along a contact zone in French Southern Alps. The rally call emitted during pair formation, could play an important role in species recognition, acting as a behavioral reproductive isolating mechanism between males and females. In the present study, the coding system of the rally call was investigated from captive males of the two species and from F1 hybrids. By playing-back natural signals, we found that the two species as well as hybrid males responded to Alectoris signals but not to another species belonging to the Phasianidae family (Colinus virginianus). Results also indicate that red-legged and rock partridges responded stronger to conspecific calls than to heterospecific ones. However, they reacted similarly to conspecific and hybrid calls. F1 hybrids responded stronger to hybrids calls than to the two species ones. They did not distinguish the two parental species signals from each other. Although the two species showed the ability to discriminate the conspecific from the heterospecific signal, they clearly responded to the other species. This behaviour may play a role in the hybridization phenomenon.     

No species barrier by call in an avian hybrid zone between California and Gambel's quail (Callipepla californica and C. gambelii)

Acoustic signals sometimes act as premating isolating barriers between animal species, but we know little about the circumstances that dictate the presence and strength of these barriers. Among insects, barriers to backcrossing are strengthened by acoustic signals that are under genetic control. Hybrid signals tend to be intermediate to parental signals, and signals are recognized only by like‐types, which results in reinforced species boundaries. This is not typically the case in avian taxa. Instead, acoustic signal transmission is controlled by some combination of genes and learning, and perhaps as a consequence of this variation, vocalizations play a diversity of roles in avian hybrid zones. I used California and Gambel's quail (Callipepla californica and C. gambelii), hybridizing birds that do not learn to vocalize, to explore whether genetically determined vocalizations function as a species barrier. Using spectral analysis, I measured temporal features of calls of uniquely colour‐banded quail that were recorded across one area of the California and Gambel's quail hybrid zone. Species discrimination is known to occur under captive conditions, though its basis is unexplored. Here I show that differences in the calls of parental species are likely great enough to permit species discrimination. Hybrid call components were intermediate to those of the parental species and covaried with genetic traits, as assessed with seven highly polymorphic microsatellite loci. Contrary to expectation, males as frequently called in response to unlike‐ as like‐type females who had initiated antiphonal calling, which is a courtship call between a female and a male. Furthermore, paired males and females did not share like‐type assembly calls, nor was there a correlation between the female's genetic or plumage traits and her mate's advertisement call. Based on these results, I conclude that California and Gambel's quail recognize each other and hybrids as potential mates and backcrossing occurs frequently. Thus, compatible mating signals could contribute to increased mixing of gene pools and slow the rate of speciation. I suggest that selection to respond to wide signal variation within species and imprinting on calls of mixed‐species coveys may cause mating signal compatibility between classes within the area of hybridization. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 86 , 253–264.     

Maternal effects and heterosis influence the fitness of plant hybrids

Here we tested two possible nonexclusive explanations for the maintenance of a hybrid swarm between Senecio jacobaea and Senecio aquaticus; first, that genotype-by-environment interactions involving water and nutrient clines are involved in hybrid fitness, and second, heterosis in early hybrid generations may provide an initial hybrid advantage that contributes to hybrid persistence. In three climate chamber studies, fitness and root growth were measured for parental species and natural and artificial F1 hybrids, in order to determine whether hybrids occur in habitats where they are more fit than parental species. Natural hybrids, which are generally back-crossed to S. jacobaea, always equaled S. jacobaea in growth characteristics. Maternal effects played a role in the fitness of F1 hybrids, with offspring from S. jacobaea mothers exhibiting higher fitness than those from S. aquaticus mothers, and compared with parental species and natural hybrids. Natural hybrids are not distributed in zones where they are most fit with respect to nutrient and water regimes. Superior fitness of early generation hybrids may contribute to hybrid swarm stability.     

Assortative preferences and discrimination by females against hybrid male song in the grasshoppers Chorthippus brunneus and Chorthippus jacobsi (Orthoptera: Acrididae)

The grasshoppers Chorthippus brunneus and Chorthippus jacobsi are highly differentiated for male mating signals, and form a mosaic hybrid zone in northern Spain. At some sites within this zone, many hybrids are observed. At others, few hybrids are observed. Such bimodal sites may reflect recent contacts between parental genotypes, or local variation in levels of assortative mating or selection against hybrids. Playback of 12 parental and F1 male songs to 296 parental and hybrid females revealed positive assortative preferences in C. brunneus and C. jacobsi females, supporting a direct role of male mating signals in female choice. However, all female genotypic classes showed reduced responsiveness to F1 male songs. Such sexual selection against hybrids is consistent with the narrow cline width observed in the field for song characters relative to morphology. These results have implications for the genetic structure of the hybrid zone and for models of speciation by reinforcement.     

Fertility in first-generation hybrids of roach, Rutilus rutilus (L.), and silver bream, Blicca bjoerkna (L.)

Fertility in first‐generation hybrids of roach, Rutilus rutilus, and silver bream, Blicca bjoerkna, was investigated. Sperm and egg production of hybrids at first sexual maturity were examined. Eggs from female hybrids were artificially fertilized with the sperm of a corresponding hybrid male; a hybrid male from the reciprocal crossbreeding; a parental species male R. rutilus; and a parental species male B. bjoerkna. The results revealed that gametogenesis was normal in female hybrids. However, in male hybrids, a low efficiency of gametogenesis was observed. The semen of male hybrids was extremely dilute, with spermatozoa concentration lower than that in parental species. Nevertheless, these F1 hybrids (males and females) from reciprocal crossbreeding were fertile. F2 and backcross generations were produced, but F2 crosses from the female hybrid and corresponding hybrid male displayed a drastically slower hatching rate. Also higher proportions of deformed embryos were hatched than in other post‐F1‐generation crosses.     

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.     

POLLEN TRANSFER BY NATURAL HYBRIDS AND PARENTAL SPECIES IN AN IPOMOPSIS HYBRID ZONE

Models of hybrid zones differ in their assumptions about the relative fitnesses of hybrids and the parental species. These fitness relationships determine the form of selection across the hybrid zone and, along with gene flow, the evolutionary dynamics and eventual outcome of natural hybridization. We measured a component of fitness, export and receipt of pollen in single pollinator visits, for hybrids between the herbaceous plants Ipomopsis aggregata and I. tenuituba and for both parental species. In aviary experiments with captive hummingbirds, hybrid flowers outperformed flowers of both parental species by receiving more pollen on the stigma. Although hummingbirds were more effective at removing pollen from anthers of I. aggregata, hybrid flowers matched both parental species in the amount of pollen exported to stigmas of other flowers. These patterns of pollen transfer led to phenotypic stabilizing selection, during that stage of the life cycle, for a stigma position intermediate between that of the two species and to directional selection for exserted anthers. Pollen transfer between the species was high, with flowers of I. aggregata exporting pollen equally successfully to conspecific and I. tenuituba flowers. Although this study showed that natural hybrids enjoy the highest quality of pollinator visits, a previous study found that I. aggregata receives the highest quantity of pollinator visits. Thus, the relative fitness of hybrids changes over the life cycle. By combining the results of both studies, pollinator-mediated selection in this hybrid zone is predicted to be strong and directional, with hybrid fitness intermediate between that of the parental species.     

Isolation mechanisms in closely related grasshopper species <Emphasis Type="Italic">Chorthippus albomarginatus</Emphasis> and <Emphasis Type="Italic">Ch. oschei</Emphasis> (Orthoptera: Acrididae)

Two closely related grasshopper species Chorthippus albomarginatus and Ch. oschei are known to hybridize in the narrow contact zone at the territory of Ukraine and Moldova. Different isolaton mechanisms providing reproductive isolation between the two species were studied. In choice mating experiments, females of the both species demonstrated a strong assortative mating (80–90% preference for the conspecific males). Comparison of the parental and hybrid viability revealed a reduced hatching and increased larval mortality in F₁ and F₂ hybrids. In choice mating experiments, the hybrid females mated less assortatively than the parental females. An assymmetry was found in mating preferences and in viability of hybrids. The results demonstrate the existence of pre-and post-mating isolation between Ch. albomarginatus and Ch. oschei. A possible fate of the hybrid zone is discussed.     

Sperm length divergence as a potential prezygotic barrier in a passerine hybrid zone

The saltmarsh sparrow Ammospiza caudacuta and Nelson''s sparrow A. nelsoni differ in ecological niche, mating behavior, and plumage, but they hybridize where their breeding distributions overlap. In this advanced hybrid zone, past interbreeding and current backcrossing result in substantial genomic introgression in both directions, although few hybrids are currently produced in most locations. However, because both species are nonterritorial and have only brief male–female interactions, it is difficult to determine to what extent assortative mating explains the low frequency of hybrid offspring. Since females often copulate with multiple males, a role of sperm as a postcopulatory prezygotic barrier appears plausible. Here, we show that sperm length differs between the two species in the hybrid zone, with low among‐male variation consistent with strong postcopulatory sexual selection on sperm cells. We hypothesize that divergence in sperm length may constitute a reproductive barrier between species, as sperm length co‐evolves with the size of specialized female sperm storage tubules. Sperm does not appear to act as a postzygotic barrier, as sperm from hybrids was unexceptional.     

Effects of hybridization on the immunity of collared Ficedula albicollis and pied flycatchers F. hypoleuca, and their infection by haemosporidians

Because they are ubiquitous and typically reduce the fitness of hosts, parasites may play important roles in hybrid zone dynamics. Despite much work on herbivores and hybrid plants, the effect of parasites on the fitness of animal hybrids is poorly known. In an attempt to partly fill this gap, we examined the prevalence of avian haemosporidians Haemoproteus in a hybrid zone between collared Ficedula albicollis and pied flycatchers F. hypoleuca . 40 species-informative genetic markers allowed us to identify F1 hybrids, thus avoiding problems inherent in many studies that group hybrid genotypes. Furthermore, naturally occurring extra-pair paternity allowed us to test the immune responses of pure and hybrid nestlings to a novel antigen (phytohaemagglutinin) in a shared environment. In contrast to previous suggestions that animal hybrids may more often display resistance against parasites than plant hybrids, F1 hybrids exhibited prevalence of parasitism and immune responses that were intermediate between the two parental species. We also detected differences between the two parental species in their prevalence of infection, with the competitively dominant species (collared flycatcher) being less often infected by Haemoproteus . Overall, our results contribute to other recent data supporting the idea that the resistance of animals to parasites is variously and unpredictably affected by hybridization, and that there is a concordance in the general patterns observed in plants and animals. Haemosporidians in avian hybrids provide a useful system for investigating the interactions between hosts and parasites that characterize host contact zones.     

Behavioral sterility of hybrid males in acoustically communicating grasshoppers (Acrididae,Gomphocerinae)

The effectiveness of hybridization barriers determines whether two species remain reproductively isolated when their populations come into contact. We investigated acoustic mating signals and associated leg movements responsible for song creation of hybrids between the grasshopper species Chorthippus biguttulus and C. brunneus to study whether and how songs of male hybrids contribute to reproductive isolation between these sympatrically occurring species. Songs of F1, F2, and backcross hybrids were intermediate between those of both parental species in terms phrase number and duration. In contrast, species-specific syllable structure within phrases was largely lost in hybrids and was produced, if at all, in an irregular and imperfect manner. These divergences in inheritance of different song parameters are likely the result of incompatibility of neuronal networks that control stridulatory leg movements in hybrids. It is highly probable that songs of hybrid males are unattractive to females of either parental species because they are intermediate in terms of phrase duration and lack a clear syllable structure. Males of various hybrid types (F1, F2, and backcrosses) are behaviorally sterile because their songs fail to attract mates.     

Mating preference of female zebrafish, Danio rerio, in relation to male dominance

Mating success tends to be skewed toward dominant males, thoughfemale mate preferences may not always correlate with male dominance.In this study, we investigated the mating preferences of femalezebrafish, Danio rerio, in the absence of male–male competition.We paired females sequentially with males of known dominancerank, using a nested, repeated measures design, with egg productionas a measure of female mate preference. We predicted that femaleswould spawn more frequently and produce larger clutches whenpaired with males of higher dominance rank. We found significantdifferences among females in the size of clutches produced andamong males in the size of clutches received, but these differenceswere independent of male dominance rank. Male body size wasnot related to either dominance rank or clutch size received.These results indicate that females vary clutch size in relationto the males with which they are paired but that they do notfavor dominant males. Thus, male competition may normally overridefemale mate preference in zebrafish.     

Genotype, soil type, and locale effects on reciprocal transplant vigor, endophyte growth, and microbial functional diversity of a narrow sagebrush hybrid zone in Salt Creek Canyon, Utah

When addressing the nature of ecological adaptation and environmental factors limiting population ranges and contributing to speciation, it is important to consider not only the plant's genotype and its response to the environment, but also any close interactions that it has with other organisms, specifically, symbiotic microorganisms. To investigate this, soils and seedlings were reciprocally transplanted into common gardens of the big sagebrush hybrid zone in Salt Creek Canyon, Utah, to determine location and edaphic effects on the fitness of parental and hybrid plants. Endophytic symbionts and functional microbial diversity of indigenous and transplanted soils and sagebrush plants were also examined. Strong selection occurred against the parental genotypes in the middle hybrid zone garden in middle hybrid zone soil; F(1) hybrids had the highest fitness under these conditions. Neither of the parental genotypes had superior fitness in their indigenous soils and habitats; rather F(1) hybrids with the nonindigenous maternal parent were superiorly fit. Significant garden-by-soil type interactions indicate adaptation of both plant and soil microorganisms to their indigenous soils and habitats, most notably in the middle hybrid zone garden in middle hybrid zone soil. Contrasting performances of F(1) hybrids suggest asymmetrical gene flow with mountain, rather than basin, big sagebrush acting as the maternal parent. We showed that the microbial community impacted the performance of parental and hybrid plants in different soils, likely limiting the ranges of the different genotypes.