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Hybridization in geese: a review

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Abstract

The high incidence of hybridization in waterfowl (ducks, geese and swans) makes this bird group an excellent study system to answer questions related to the evolution and maintenance of species boundaries. However, knowledge on waterfowl hybridization is biased towards ducks, with a large knowledge gap in geese. In this review, we assemble the available information on hybrid geese by focusing on three main themes: (1) incidence and frequency, (2) behavioural mechanisms leading to hybridization, and (3) hybrid fertility. Hybridization in geese is common on a species-level, but rare on a per-individual level. An overview of the different behavioural mechanisms indicates that forced extra-pair copulations and interspecific nest parasisitm can both lead to hybridization. Other sources of hybrids include hybridization in captivity and vagrant geese, which may both lead to a scarcity of conspecifics. The different mechanisms are not mutually exclusive and it is currently not possible to discriminate between the different mechanisms without quantitative data. Most hybrid geese are fertile; only in crosses between distantly related species do female hybrids become sterile. This fertility pattern, which is in line with Haldane’s Rule, may facilitate interspecific gene flow between closely related species. The knowledge on hybrid geese should be used, in combination with the information available on hybridization in ducks, to study the process of avian speciation.

Background

Hybridization, interbreeding of species, has always intrigued ornithologists. Ernst Mayr [1] pointed out that “In birds, we have a fair amount of information, since some collectors, sensing their scarcity value, have specialized in the collecting of hybrids, and amateur observers have always been fascinated by them.” The first attempt to compile the numerous scattered references and reports of avian hybrids was undertaken by Suchetet [2]. Later on, many more checklists and compilations of avian hybrids have been published [310]. The incidence of hybridization varies among bird orders, with the Anseriformes (waterfowl: ducks, geese and swans) showing the highest propensity to hybridize. Over 60 % of waterfowl species has hybridized with at least one other species and this figure increases to almost 77 % when including captive hybrids [8].

The high incidence of hybridization in waterfowl makes this bird group an excellent study system to answer questions related to the origin and preservation of species. For example, how do waterfowl species remain distinct despite high levels of hybridization? Does hybridization lead to the exchange of genetic material (i.e., introgression) and if so, does this provide individuals with an adaptive advantage or disadvantage? Indeed, there are still many open questions in speciation and hybridization research that could be answered by studying hybridization in waterfowl [11, 12]. These questions, however, are not the focus of this review.

The knowledge on waterfowl hybridization is biased towards ducks, as illustrated by an extensive inventory of hybrid ducks [13], an analysis of hybrid duck fertility patterns [14] and several genetic studies documenting interspecific gene flow due to introgressive hybridization (e.g., [1517]). The knowledge of goose hybrids is clearly lagging behind. Several studies reported goose hybrids [1821] or provided a description of local records of hybrid geese [2224], but no study has been dedicated to the incidence of goose hybrids or their fertility. The differences in species discrimination and social structure between ducks and geese provide the opportunity to formulate and test research questions that will broaden our understanding on the origin and preservation of waterfowl species. For instance, how does sexual selection (as measured by the degree of sexual dimorphism) relate to the frequency of hybridization? Does hybridization accelerate of slow down the speciation process? Which behavioural and morphological characateristics determine conspecific or heterospecific mate choice? Is there strong selection against hybrids?

In this review, we address the knowledge gaps on hybrid geese by focusing on three main themes: (1) incidence and frequency, (2) behavioural mechanisms leading to hybridization, and (3) hybrid fertility.

Goose taxonomy

Table 1 gives an overview of the current taxonomic classification of the True Geese. We follow the International Ornithologists’ Union (IOU) for species names [25], with one exception. Even though IOU currently recognizes two species of Bean Goose (Taiga Bean Goose A. fabalis and Tundra Bean Goose A. serrirostris), most reports on hybridization date from before this split into two species and hence, it is not possible to analyse these Bean Goose species separately.

Table 1 Current taxonomy for the True Geese (tribe Anserini)

Incidence and frequency of goose hybrids

There is an important distinction between incidence and frequency of hybridization. Incidence is binary: a certain hybrid combination has been observed or not. Figure 1 gives an overview of 74 observed hybrid geese in nature and captivity, based on records retrieved from the Serge Dumont Hybrid Database [26]. The frequency of hybridization refers to the number of hybrid individuals in the wild. Because actual numbers of hybrids are mostly not included in bird counts and some crosses are very hard to identify [27], it is nearly impossible to get an accurate estimation of the number of hybrids for certain combinations of species. However, two surveys in Great Britain monitored the frequency of hybrid geese in 1991 and 2000 when occurrence of the most common hybrid (Canada Goose x Greylag Goose) was quantified. These hybrids represent less than one per cent of the British population of Canada Geese and Greylag Geese (0.33 % in 1991 and 0.11 % in 2000) [28, 29], falling in line with previous estimates from other bird groups [13, 3032].

Fig. 1
figure1

Overview of incidence of hybridization in geese. Hybridization in nature is depicted above the diagonal, whereas hybridization in captivity below the diagonal. Species that hybridized both in nature and in captivity are included only in the former category

Several European studies have compiled the occurrence of hybrid geese based on data from a variety of sources, such as regional and local bird magazines or personal observations (Table 2). In all studies, hybrids between Canada Goose and Greylag Goose were most numerous, while other hybrid geese were limited to a handful of individuals [23, 24, 29]. It seems that hybridization in geese is common on a species-level (Fig. 1), but rare on a per-individual level (Table 2). Although hybrids are rare in populations, a few hybrids can provide a bridge for interspecific gene flow [33], which can have important evolutionary consequences, such as adaptive introgression [34].

Table 2 Frequency of hybrid geese recorded in three countries: Germany [67], Great Britain [29] and Sweden [23]

Origin of goose hybrids

Several behavioural mechanisms have been called upon to explain the production of hybrid offspring in birds [3537]. Here, we discuss four mechanisms that are relevant for the occurrence of goose hybrids, namely (1) nest parasitism, (2) extra-pair copulations, (3) rarity of conspecifics, and (4) captive birds.

Nest parasitism

Nest parasitism and brood amalgamation occur commonly in waterfowl, both within and among species [3840]. Intraspecific nest parasitism has been documented for several goose species (Table 3), but only three goose species are known to show interspecific nest parasitism, namely Greylag Goose, Snow Goose and Canada Goose [23, 41]. Interspecific nest parasitism could facilitate hybridization because hatching by a heterospecific foster parent might lead to sexual imprinting on the foster parent’s species and this may in turn lead to interspecific mate choice in the future (Fig. 2). The plausibility of this scenario has been assessed experimentally by means of cross-fostering experiments: Fabricius [42] placed eggs of Greylag Geese in the nest of Canada Geese. The young Greylag Geese followed their foster parents to their wintering grounds. On return, all females (16) paired with Greylag Geese, whereas 5 out of 19 males paired with Canada Geese. Furthermore, some Greylag Goose males that lost a partner remated with a female Canada Goose, showing that these males were sexually imprinted on this species.

Table 3 Occurrence of intra- and interspecific nestparastism and extra-pair copulations in all goose species
Fig. 2
figure2

Graphical representation showing how interspecific nest parasitism can lead to hybridization

Some goose species adopt conspecific young [4347]. Whether geese also adopt heterospecific goslings and if this adoption can affect sexual imprinting and future mate choice is unknown. Heterospecific adoption has been documented between several distantly related bird species, but seems to be a rare phenomenon [48].

Extra-pair copulations

Forced extra-pair copulations (often called “rapes”) have been reported in several species of waterfowl [49]. Trivers [50] suggested that such extrapair copulations could be functional; he noted that “a mixed strategy will be the optimal male course – to help a single female raise young, while not passing up opportunities to mate with other females whom he will not aid.” Males of several goose species engage in forced extra-pair copulations, such as Greater White-fronted Goose [51], Brent Goose [52] and Canada Goose [53]. But this behaviour has been studied most extensively in Snow Goose and Ross’ Goose [5456]. In the Canadian Karrak Lake Colony, Dunn et al. [55] observed that among successful copulations, 33 and 38 % were extra-pair in Ross’ and Snow Geese, respectively. Despite this high precentage of extra-pair copulations, only 2–5 % of the goslings had another father than the male guarding the nest. A similar low percentage of extrapair paternity (2–4 %) was also reported for Snow Geese in northern Manitoba, Canada [54]. Based on these low ferilization percentages, forced extra-pair copulations appear to be a relatively inefficient reproductive tactic for males of these goose species. However, offspring resulting from successful extrapair copulations do provide a fitness benefit to males.

Extra-pair copulations can lead to hybridization when males copulate with females of another species. This has been observed for ducks: for instance, Seymour [57] reports three occasions of an extra-pair copulation attempt by a male Mallard (Anas platyrhynchos) on a female Black Duck (A. rubripes). However, interspecific extra-pair copulations have not been documented in geese. This can be due to the limited number of behavioural studies of geese during the period when copulations are most likely, and may also reflect differences in species discrimination and social structure between ducks and geese [49]. Male ducks often seem unable or indifferent to discriminate between females of different species (which look very similar) as many studies report male ducks displaying to heterospecific females [36, 58, 59]. The social structure of geese, with long-term pairbonds and nest guarding by males, limits the opportunties for males to seek extra-pair copulations [60]. Although interspecfic extra-pair copulations can potentially result in hybrid offspring, this behavioural mechanism seems of minor importance in the origin of hybrid geese, because of its low frequency and the low fertilization rate of such extra-pair copulations. This conclusion is in line with the study by Randler [61], who showed that “interspecific brood amalgamation has a stronger impact on natural hybridization in wildfowl than forced extra-pair copulations.”

Scarcity of conspecifics

Hubbs’ Principle or the Desparation Hypothesis states that the rarer species is more likely to mate with heterospecifics [62]. There are several situations in which individual birds can be confronted with a scarcity of conspecifics, such as range expansion, vagrant birds or the release/escape of captive birds in a non-native environment. With regard to geese, range expansion should include an expansion of the wintering grounds, where mate choice occurs [63]. Some birds will “make the best out of a bad job” and pair with a heterospecific mate: hybridizing with a closely related species may be a better solution than remaining unpaired [37, 64]. For instance, Indigo Buntings (Passerina cyanea) and Lazuli Buntings (P. amoena) switched to heterospecifics when no conspecific mates were available [64]. Another good example of the Desparation Hypothesis concerns two duck species on the Falkland Islands, where Speckled Teals (Anas flavirostris) outnumber Yellow-billed Pintails (A. georgica) about ten to one. This numerical imbalance leads to hybridization [65]. The Desperation Hypothesis is not restricted to natural situations, in captivity birds are often confronted with a scarcity of conspecifics and might choose to mate with the available heterospecifics.

Captive birds

Cockrum [3] already noted that “If hybrids resulting from birds in captivity were listed, the list would be much larger, especially among ducks and geese.” Indeed, numerous hybrids have been produced in captivity [8]. The occurrence of hybridization in captivity can be explained by the mechanisms discussed above, namely extra-pair copulations, nest parasitism and scarcity of conspecifics. When these hybrids escape, they can be mistakenly reported as wild hybrids. However, it may be possible to deduce the captive origin of hybrids when one of the parent species is not native by examining the range of occurrence. Table 2 shows that many hybrid geese probably have captive origin; for instance, some of the most common hybrids in Europe are between Greylag Goose and two introduced species, Canada Goose and Swan Goose. However, there is also the possibility that vagrant geese enter the range of other species. For example, North American Snow Geese are occasionally observed in Europe during migration [66] and hybrids between Snow Goose and several European species have been reported [10].

Randler [67] introduced the “captivity effect” to account for the high rates of Anser hybrids in released populations. He argued that domestication of Greylag Goose and Swan Goose has resulted in genetical impoverishment and unnatural behaviour, leading to a relatively strong tendency for hybridization. For example, in Greylag Geese, the frequency of hybrids was higher in naturalised compared to natural populations [23, 67, 68]. The effects of captivity on hybridization should thus be taken into account.

Fertility of goose hybrids

In The Origin of Species, Darwin [69] discussed the fertility of hybrids between two domesticated goose species, the Greylag Goose and the Swan Goose:

“The hybrids from the common and Chinese geese (A. cygnoides), species which are so different that they are generally ranked in distinct genera, have often bred in this country with either pure parent, and in one single instance they have bred inter se. This was effected by Mr Eyton, who raised two hybrids from the same parents but from different hatches; and from these two birds he raised no less than eight hybrids (grandchildren of the pure geese) from one nest. In India, however, these cross-bred geese must be far more fertile; for I am assured by two eminently capable judges, namely Mr Blyth and Capt. Hutton, that whole flocks of these crossed geese are kept in various parts of the country; and as they are kept for profit, where neither pure parent-species exists, they must certainly be highly fertile.”

Later, he repeated the experiment of Mr. Eyton by crossing “a brother and sister hybrid from the same hatch” that he received from Rev. Goodacre [70]. He only managed to rear five hybrids (several eggs did not hatch or remained unfertilized), but he was still startled by “the fact that these two species of geese [are] breeding so freely together.” He attributed the fertility of these hybrids to the long history of goose domestication. We now know that, irrespective of domestication, the potential for hybridization is lost slowly on an evolutionary timescale in birds, [71] and that many bird species are capable of producing fertile hybrids [72].

The evolution of hybrid sterility and inviability (both caused by postzygotic incompatibilities) has been studied in Drosophila [73], frogs [74], butterflies [75] and birds [72]. These studies showed an increase of postzygotic isolation between species with divergence time. Furthermore, the evolution of postzygotic incompatibility follows Haldane’s Rule [76], which states that “when in the F1 offspring of two different animal races one sex is absent, rare, or sterile, that sex is the heterozygous [or heterogametic] sex”. In birds, where sex is determined by a ZZ/ZW system, females are the heterogametic sex and hybrid females are thus expected to show greater fitness reductions compared to male hybrids. This expectation has been confirmed for birds in general [72], but also for specific bird groups, including ducks [14], galliform birds [77] and pigeons and doves [78].

One of the possible mechanisms that has been invoked to explain Haldane’s rule is dominance theory, which is based on the Dobzhansky-Muller incompatibility model [79, 80]. Dominance theory states that hybrid sterility and unviability are the outcome of the interaction of two (or more) genes that have developed incompatible alleles in allopatry. If these alleles are recessive and located on the Z-chromosome, their effect will be much larger in female birds because this sex lacks another Z-chromosome that could hold a dominant version of the incompatible allele, which would nullify the negative effect of the recessive one. Moreover, it has been suggested that the Z-chromosome plays a disproportionately large role in the development of intrinsic incompatibilities [81]. Several lines of evidence support this “Large Z-effect.” First, Z-linked genes evolve faster compared to autosomal loci (“Faster Z-effect”), thereby speeding up the accumulation of incompatible alleles on this sex chromosome [82, 83]. Second, if genes involved in premating and postzygotic isolation both occur on the Z-chromosome and thus become physically linked, it is expected that this facilitates the evolution of isolation barriers by means of reinforcement [84]. This situation has been described for Ficedula flycatchers, where genes for female preference and low hybrid fitness are located on the Z-chromosome [85, 86].

We tested whether geese also conform to Haldane’s Rule. We obtained cytochrome b sequences from GENBANK and calculated genetic distances between taxa using the Maximum Composite Likelihood model with Gamma Distribution in MEGA6 [87]. Reports on hybrid goose fertility were collected from the Handbook of Avian Hybrids of the World [10]. We performed a logistic regression in SPSS (version 19.0) with hybrid fertility as dependent variable (0 = both sexes fertile, 1 = only males fertile) and genetic distance as independent variable. To our knowledge, there are no reports of goose hybrids where only the females are fertile.

At high genetic distances, for most species only male hybrids are fertile (Fig. 3, ß = 53.425, SE = 25.485, z-value = 2.096, p = 0.0361), a pattern that is consistent with Haldane’s Rule. Two species pairs deviate from the expected pattern: only male hybrids between the congeneric Greater White-fronted Goose and Swan Goose are fertile and both sexes are fertile when crossing the more distantly related Canada Goose and Greater White-fronted Goose. However, a more detailed analysis is necessary to fully understand the evolution of postzygotic incompatibilities in geese. For example, Lijtmaer et al. [78] studied postzygotic isolation in pigeons and doves based on records of old interspecific breeding experiments [88], that included data on the number of unhatched eggs and the sex ratio of clutches. Such analyses provide insights, not only into the fertility of hybrids, but also into the fertility and viability of backcrosses. For instance, Arrieta et al. [77] showed that hybrid inviability was higher in F2 compared to F1 hybrids in galliform birds, indicating that interspecific gene flow may be hampered due to inviable F2 hybrids. For geese, the fertility of male birds at high genetic distances suggests the possibility of interspecific gene flow between distantly related species (e.g., Greylag Goose and Canada Goose), but if consequent backcrosses are sterile or inviable, then the possibility of interspecific gene flow is greatly reduced. On the other hand, the fertility of hybrids at low genetic distances (e.g., Greater White-fronted Goose and Greylag Goose) provides the opportunity of interspecific gene flow between closely related species. For example, Leafloor et al. [89] reported gene flow between Canada Goose and Cackling Goose across an arctic hybrid zone.

Fig. 3
figure3

Fertility of goose hybrids at different genetic distances (based on cytochrome b sequences). At high genetic distances only male hybrids are fertile, a pattern in accordance with Haldane’s Rule

Conclusions

Hybridization in geese is common on a species-level, but rare on a per-individual level. The origin of the occasional hybrids is difficult to determine. An overview of the different mechanisms shows that, in theory, interspecific nest parasisitm or forced extra-pair copulations could lead to hybridization. Other sources of hybrids include a scarcity of conspecifics, hybridization in captivity and vagrant geese. The different mechanisms are not mutually exclusive, for instance, certain hybrids might be the result of extra-pair copulations in captivity. Currently, it is not possible to discriminate between the different mechanisms without quantitative data. To unravel the relative importance of these mechanisms, field data should be collected and experiments could be conducted in captivity. For example, the frequency of interspecific nest parasitism and extra-pair copulations may be documented in mixed breeding colonies. The occurrence of possible hybrids (which can be identified by means of genetic tests) in such colonies can then be related to the frequency of these behaviours. In captivity, experiments can be set up to observe how different goose species react to a scarcity of conspecifics and the availability of diverse heterospecifics. Most goose hybrids are fertile; only at high genetic distances do female hybrids become sterile. This fertility pattern provides the opportunity for interspecific gene flow between closely related species.

The overview of hybridization in geese presented here can be used, in combination with the knowledge available on duck hybrids, to study the process of avian speciation. Moreover, the differences in species discrimination and social structure between ducks and geese provide the opportunity to formulate and test research questions that will broaden our understanding on the origin and preservation of species.

References

  1. 1.

    Mayr E. Systematics in the origin of species : from the viewpoint of a zoologist, Columbia biological, vol. 13. New York: Harvard University Press; 1942.

  2. 2.

    Suchetet A. In: Librairie JB, editor. Des hybrides a l’etat sauvage. Regne animal. Tome premier. Classe des oiseaux. Paris: Bailliere et fils; 1897.

  3. 3.

    Cockrum EL. A check-list and bibliography of hybrid birds in North America north of Mexico. Wilson Bull. 1952;64(3):140–59.

  4. 4.

    Meise W. Naturliche bastardpopulationen und speziationprobleme bei vogels, Abhandlungen aus dem Gebiete der Naturwissenschaften, Herausgegeben von dem naturwissenschaftlichen Verein in Hamburg. 1975. p. 18–9. 187–254.

  5. 5.

    Gray AP, Bird hybrids: a check-list with bibliography. Technical communication of the Commonwealth Bureau of Animal Breeding and Genetics; no. 13. 1958, Bucks: CAB.

  6. 6.

    Grant PR, Grant BR. Hybridization of bird species. Science. 1992;256(5054):193–7.

  7. 7.

    Panov E. Natural hybridization and ethological isolation in birds. Moscow: Nauka; 1989.

  8. 8.

    Ottenburghs J et al. The avian hybrids project: gathering the scientific literature on avian hybridization. Ibis. 2015;157(4):892–4.

  9. 9.

    Mayr E, Short LL. Species taxa of North American birds; a contribution to comparative systematics, vol. 9. Cambridge: Publications of the Nuttall Ornithological Club; 1970. Mass.,: The Club. 127 p.

  10. 10.

    McCarthy EM. Handbook of avian hybrids of the world. Oxford: Oxford University Press; 2006. p. 583. xiv.

  11. 11.

    Abbott R et al. Hybridization and speciation. J Evol Biol. 2013;26(2):229–46.

  12. 12.

    Butlin R et al. What do we need to know about speciation? Trends Ecol Evol. 2012;27(1):27–39.

  13. 13.

    Gillham E, Gillham B. Updating hybrid ducks: a contribution towards an inventory. E.H. & B.L. Gillham; Published by the authors. 1998

  14. 14.

    Tubaro PL, Lijtmaer DA. Hybridization patterns and the evolution of reproductive isolation in ducks. Biol J Linn Soc. 2002;77(2):193–200.

  15. 15.

    Kraus RHS, et al. Widespread horizontal genomic exchange does not erode species barriers among sympatric ducks. BMC Evol. Biol. 2012;12(1):45.

  16. 16.

    Peters JL et al. Interspecific hybridization contributes to high genetic diversity and apparent effective population size in an endemic population of mottled ducks (Anas fulvigula maculosa). Conserv Genet. 2014;15(3):509–20.

  17. 17.

    Lavretsky P, McCracken KG, Peters JL. Phylogenetics of a recent radiation in the mallards and allies (ayes: anas): inferences from a genomic transect and the multispecies coalescent. Mol Phylogenet Evol. 2014;70:402–11.

  18. 18.

    Delnicki D. Ross goose snow goose hybrid in south Texas. Auk. 1974;91(1):174.

  19. 19.

    Craven SR, Westemeier RL. Probable Canada goose X white-fronted goose hybrids. Wilson Bull. 1979;91(4):628–9.

  20. 20.

    Weckstein JD et al. Hybridization and population subdivision within and between Ross’s geese and lesser snow geese: a molecular perspective. Condor. 2002;104(2):432–6.

  21. 21.

    Nijman V, Aliabadian M, Roselaar CS. Wild hybrids of lesser white-fronted goose (anser erythropus) x greater white-fronted goose (a. Albifrons) (Aves: anseriformes) from the European migratory flyway. Zool Anz. 2010;248(4):265–71.

  22. 22.

    Bloomfield A. Hybrid and aberrant geese in Britain. Birding World. 2004;17(3):123–7.

  23. 23.

    Kampe-Persson H, Lerner H. Occurrence of hybrid geese in Sweden – a conservation problem? Ornis Svecica. 2007;17:154–86.

  24. 24.

    Randler C. Hybrid wildfowl in central Europe - an overview. Waterbirds. 2008;31(1):143–6.

  25. 25.

    Gil F, Donsker D. IOC World Bird List (v 3.3). Available at http://www.worldbirdnames.org. 2013 26-03-2013].

  26. 26.

    Dumont, S. Serge Dumont Bird Hybrids Database: http://www.bird-hybrids.com/. 2014.

  27. 27.

    Randler C. Frequency of bird hybrids: does detectability make all the difference? J Ornithol. 2004;145(2):123–8.

  28. 28.

    Delany SN. Survey of Introduced Geese in Britain, Summer 1991: Provisional Results. Un published report to JNCC, Central Science Laboratory and National Trust. WWT, Slimbridge, 1992.

  29. 29.

    Rowell HE et al. The Naturalised Goose Survey 2000. 2004, Slimbridge: WWT. 28

  30. 30.

    Parmenter T, Byers C. A guide to the warblers of the western Palaearctic. Cornell University: Bruce Coleman Books; 1991.

  31. 31.

    Curson J, Beadle D, Quinn D. New World Warblers. London: A&C Black;2010.

  32. 32.

    Harrap S, Quinn D, Tits. Nuthatches and Treecreepers. London: A&C Black;2010

  33. 33.

    Mallet J. Hybridization as an invasion of the genome. Trends Ecol Evol. 2005;20(5):229–37.

  34. 34.

    Hedrick PW. Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Mol Ecol. 2013;22(18):4606–18.

  35. 35.

    Wirtz P. Mother species-father species: unidirectional hybridization in animals with female choice. Anim Behav. 1999;58:1–12.

  36. 36.

    Randler C. Avian hybridization, mixed pairing and female choice. Anim Behav. 2002;63:103–19.

  37. 37.

    Randler C. Behavioural and ecological correlates of natural hybridization in birds. Ibis. 2006;148(3):459–67.

  38. 38.

    Eadie JM, Kehoe FP, Nudds TD. Pre-hatch and post-hatch brood amalgamation in north-American anatidae - a review of hypotheses. Canadian J Zool Revue Canadienne De Zoologie. 1988;66(8):1709–21.

  39. 39.

    Rohwer FC, Freeman S. The distribution of conspecific nest parasitism in birds. Canadian J Zool-Revue Canadienne De Zoologie. 1989;67(2):239–53.

  40. 40.

    Beauchamp G. Determinants of intraspecific brood amalgamation in waterfowl. Auk. 1997;114(1):11–21.

  41. 41.

    Beauchamp G. The relationship between intra- and interspecific brood amalgamation in waterfowl. Condor. 1998;100(1):153–62.

  42. 42.

    Fabricius E. Interspecific mate choice following cross-fostering in a mixed colony of greylag geese (anser anser) and Canada geese (branta Canadensis) - a study on development and persistence of species preferences. Ethology. 1991;88(4):287–96.

  43. 43.

    Larsson K, Tegelstrom H, Forslund P. Intraspecific nest parasitism and adoption of young in the barnacle goose - effects on survival and reproductive-performance. Anim Behav. 1995;50:1349–60.

  44. 44.

    Williams TD. Adoption in a precocial species, the lesser snow goose - intergenerational conflict, altruism or a mutually beneficial strategy. Anim Behav. 1994;47(1):101–7.

  45. 45.

    Kalmbach E. Why do goose parents adopt unrelated goslings? a review of hypotheses and empirical evidence, and new research questions. Ibis. 2006;148(1):66–78.

  46. 46.

    Choudhury S et al. Adoption of young and intraspecific nest parasitism in barnacle geese. Condor. 1993;95(4):860–8.

  47. 47.

    Zicus MC. Canada goose brood behavior and survival estimates at crex meadows. Wisconsin Wilson Bull. 1981;93(2):207–17.

  48. 48.

    Shy MM. Interspecific feeding among birds - a review. J Field Ornithol. 1982;53(4):370–93.

  49. 49.

    Mckinney F, Derrickson SR, Mineau P. Forced copulation in waterfowl. Behaviour. 1983;86:250–94.

  50. 50.

    Trivers R. Parental investment and sexual selection.  In B. Campbell, ed. Sexual Selection and the Descent of Man, 1871-1971, Aldine-Atherton, Chicago. 1972;136-179

  51. 51.

    Ely CR. Extra-pair copulation in the greater white-fronted goose. Condor. 1989;91(4):990–1.

  52. 52.

    Welsh D, Sedinger JS. Extra-pair copulations in black Brant. Condor. 1990;92(1):242–4.

  53. 53.

    Moore JA et al. The effects of anthropogenic alteration of nesting habitat on rates of extra‐pair fertilization and intraspecific brood parasitism in Canada geese branta Canadensis. Ibis. 2012;154(2):354–62.

  54. 54.

    Lank DB et al. Intraspecific nest parasitism and extra-pair copulation in lesser snow geese. Anim Behav. 1989;37:74–89.

  55. 55.

    Dunn PO et al. Forced copulation results in few extrapair fertilizations in Ross’s and lesser snow geese. Anim Behav. 1999;57:1071–81.

  56. 56.

    Mineau P, Cooke F. Rape in the lesser snow goose. Behaviour. 1979;70:280–91.

  57. 57.

    Seymour N. Forced copulation in sympatric American black ducks and mallards in nova Scotia. Can J Zool. 1990;68(8):1691–6.

  58. 58.

    Bossema I, Kruijt J. Male activity and female mate acceptance in the mallard (anas platyrhynchos). Behaviour. 1982;79(2):313–23.

  59. 59.

    Brodsky LM, Ankney CD, Dennis DG. The influence of male-dominance on social interactions in black ducks and mallards. Anim Behav. 1988;36:1371–8.

  60. 60.

    Owen M. Wild geese of the world : their life history and ecology. London: Batsford; 1980.

  61. 61.

    Randler C. Do forced extrapair copulations and interspecific brood amalgamation facilitate natural hybridisation in wildfowl? Behaviour. 2005;142:477–88.

  62. 62.

    Hubbs CL. Hybridization between fish species in nature. Syst Zool. 1955;4(1):1–20.

  63. 63.

    Rohwer FC, Anderson MG. Female-biased philopatry, monogamy, and the timing of pair formation in migratory waterfowl, in Current ornithology. New York: Springer; 1988, p. 187–221.

  64. 64.

    Baker MC. Female buntings from hybridizing populations prefer conspecific males. Wilson Bull. 1996;108(4):771–5.

  65. 65.

    McCracken KG, Wilson RE. Gene Flow and Hybridization between Numerically Imbalanced Populations of Two Duck Species in the Falkland Islands. Plos One, 2011;6.8:e23173.

  66. 66.

    Bruun B. North American waterfowl in Europe. British Birds. 1971;64:385–408.

  67. 67.

    Randler C. Wasservogelhybriden (anseriformes) im westlichen mitteleuropa - verbreitung. Auftreten und Ursachen Ökologie der Vögel. 2000;22(1):1–106.

  68. 68.

    Sibley D. A guide to finding and identifying hybrid birds. Birding. 1994;26:162–77.

  69. 69.

    Darwin C. The origin of species by means of natural selection : the preservation of favoured races in the struggle for life. London: Murray; 1859.

  70. 70.

    Darwin C. Fertility of hybrids from the common and Chinese goose. Nature. 1880;21:207.

  71. 71.

    Prager EM, Wilson AC. Slow evolutionary loss of potential for interspecific hybridization in birds - manifestation of slow regulatory evolution. Proc Natl Acad Sci U S A. 1975;72(1):200–4.

  72. 72.

    Price TD, Bouvier MM. The evolution of F-1 postzygotic incompatibilities in birds. Evolution. 2002;56(10):2083–9.

  73. 73.

    Coyne JA, Orr HA. Patterns of speciation in drosophila. Evolution. 1989;43(2):362–81.

  74. 74.

    Sasa MM, Chippindale PT, Johnson NA. Patterns of postzygotic isolation in frogs. Evolution. 1998;52(6):1811–20.

  75. 75.

    Presgraves DC. Patterns of postzygotic isolation in Lepidoptera. Evolution. 2002;56(6):1168–83.

  76. 76.

    Haldane JBS. Sex ratio and unisexual sterility in hybrid animals. J Genet. 1922;12:101–9.

  77. 77.

    Arrieta RS, Lijtmaer DA, Tubaro PL. Evolution of postzygotic reproductive isolation in galliform birds: analysis of first and second hybrid generations and backcrosses. Biol J Linn Soc. 2013;110(3):528–42.

  78. 78.

    Lijtmaer DA, Mahler B, Tubaro PL. Hybridization and postzygotic isolation patterns in pigeons and doves. Evolution. 2003;57(6):1411–8.

  79. 79.

    Wu C-I, Ting C-T. Genes and speciation. Nat Rev Genet. 2004;5(2):114–22.

  80. 80.

    Presgraves DC. The molecular evolutionary basis of species formation. Nat Rev Genet. 2010;11(3):175–80.

  81. 81.

    Presgraves DC. Sex chromosomes and speciation in Drosophila. Trends Genet. 2008;24(7):336–43.

  82. 82.

    Ellegren H. Genomic evidence for a large-Z effect. Proc R Soc B Biol Sci. 2009;276(1655):361–6.

  83. 83.

    Storchova R, Reif J, Nachman MW. Female heterogamety and speciation: reduced introgression of the Z chromosome between Two species of nightingales. Evolution. 2010;64(2):456–71.

  84. 84.

    Hall DW, Kirkpatrick M. Reinforcement and sex linkage. Evolution. 2006;60(5):908–21.

  85. 85.

    Saetre GP et al. Sex chromosome evolution and speciation in Ficedula flycatchers. Proc R Soc B Biol Sci. 2003;270(1510):53–9.

  86. 86.

    Backström N et al. A high-density scan of the Z chromosome in ficedula flycatchers reveals candidate loci for diversifying selection. Evolution. 2010;64(12):3461–75.

  87. 87.

    Tamura K et al. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9.

  88. 88.

    Whitman CO, Riddle O. Posthumous Works of Charles Otis Whitman.: Inheritance, Fertility, and the Dominance of Sex and Color in Hybrids of Wild Species of Pigeons. Washington: Carnegie Institution of Washington; 1919.

  89. 89.

    Leafloor JO, Moore JA, Scribner KT. A hybrid zone between Canada geese (branta Canadensis) and cackling geese (B. Hutchinsii). Auk. 2013;130(3):487–500.

  90. 90.

    Weigmann C, Lamprecht J. Intraspecific nest parasitism in Bar-headed geese. Anser-Indicus Animal Behaviour. 1991;41:677–88.

  91. 91.

    Cramp S, Simmons K. The birds of the western Palearctic. Vol. 1, Ostrich toducks. Oxford: UniversityPress; 1977.

  92. 92.

    Lank DB et al. Environmental and demographic correlates of intraspecific nest parasitism in lesser snow geese chen-caerulescens-caerulescens. J Anim Ecol. 1989;58(1):29–45.

  93. 93.

    Lank DB, Rockwell RF, Cooke F. Frequency-dependent fitness consequences of intraspecific nest parasitism in snow geese. Evolution. 1990;44(6):1436–53.

  94. 94.

    Syroechkovsky E. laying of eggs by white geese into strange nests. Zoologichesky zhurnal. 1979;58((7):1033–41.

  95. 95.

    Bellrose FC, Kortright, Ducks, geese & swans of North America. Harrisburg, PA: Stackpole Books; 1976.

  96. 96.

    Eisenhauer DI, Kirkpatrick CM. Ecology of emperor goose in Alaska. Wildl Monogr. 1977;57:6–62.

  97. 97.

    Prevett J, Lieff B, Macinnes C. Nest parasitism at McConnell river. NWT Can Field-Nat. 1972;86:369–72.

  98. 98.

    Seddon LM, Nudds TD. The costs of raising nidifugous offspring: brood rearing by giant Canada geese (Branta canadensis maxima). Can J Zool. 1994;72(3):533–40.

  99. 99.

    Anderholm S et al. Nest parasitism in the barnacle goose: evidence from protein fingerprinting and microsatellites. Anim Behav. 2009;78(1):167–74.

  100. 100.

    Bregnballe T, Madsen J. Post-hatching behaviour of light-bellied Brent geese branta bernicla hrota. Wildfowl. 1990;41(41):27–34.

  101. 101.

    Spaans B et al. Breeding biology of dark-bellied Brent geese branta-bernicla-bernicla in Taimyr in 1990 in the absence of arctic foxes and under favorable weather conditions. Polar Res. 1993;12(2):117–30.

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Acknowledgements

We are grateful to Milena Holmgren and Kevin D. Matson for their inspiring discussions during the development of this manuscript. We would like to thank two anonymous reviewers for their useful comments.

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Correspondence to Jente Ottenburghs.

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The authors declare that they have no competing interests.

Authors’ contributions

J.O. wrote the paper. P.v.H., S.v.W., R.C.Y. and H.H.T.P. commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Ottenburghs, J., van Hooft, P., van Wieren, S.E. et al. Hybridization in geese: a review. Front Zool 13, 20 (2016) doi:10.1186/s12983-016-0153-1

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Keywords

  • Hybridization
  • Introgression
  • Behaviour
  • Nest parasitism
  • Extra-pair copulations
  • Fertility
  • Anatidae
  • Captivity

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