bio summary

ORI GIN AL PA PER

Natural hybridization and conservation

Meritxell Genovart

Received: 16 May 2008 / Accepted: 21 November 2008 / Published online: 10 December 2008 � Springer Science+Business Media B.V. 2008

Abstract This review deals with natural hybridization, an important subject in conser- vation biology. Natural hybridization is defined as the secondary contact between two

populations that have evolved separately over a long period of time. This process is

uncommon in terms of the total number of individuals involved, but is much less unusual if

we consider the number of species that hybridize. Thus, natural hybridization may be an

important process in the shaping of the evolutionary trajectories of many plant and animal

species. The possible consequences of natural hybridization, which can either promote or

prevent evolutionary divergence between taxa and will involve many ecological factors,

are analysed here. I question whether natural hybridization poses always a problem in

conservation and try to answer when conservation biologists and managers do have a

responsibility to take decisions. Several examples of hybridization related to management

strategies are also discussed. In conclusion, I believe that it is impossible to provide

conservation managers with a simple handbook explaining how to proceed in cases of

hybridization––each case is unique and should be analyzed individually. The only advice is

that the more we know about hybridization and the factors involved, the better we will be

able to assess each situation, to establish the possible consequences and even to estimate

the probability of success of any particular conservation strategy.

Keywords Conservation � Dispersal � Evolutionary process � Hybridization � Management � Selection � Speciation

Populations that have been isolated for a long time may eventually come into contact,

giving rise to a mixed population and thus the incorporation of genes from one genetically

distinct population into another (Futuyama 1998). This secondary contact between taxa in

nature is what is known as natural hybridization. Historically, biologists (essentially

M. Genovart (&) Institut Mediterrani d’Estudis Avançats IMEDEA (CSIC-UIB), Miquel Marquès 21, Esporles, Mallorca 07190, Spain e-mail: [email protected]

123

Biodivers Conserv (2009) 18:1435–1439 DOI 10.1007/s10531-008-9550-x

zoologists and botanists) have held contrasting points of view regarding the evolutionary

role of natural hybridization. Whereas zoologists have tended to consider hybridization as

an isolated process or, rather, a taxonomical problem, botanists have regarded hybridiza-

tion as just another evolutionary process. However, more serious dilemmas appear when

analysing hybridization processes between species since, according to the most widely

used concept of species (the ‘species concept’; Mayr 1942), species are reproductively

isolated from one other and so hybridization processes should never in fact occur. The root

of the problem probably lies in the acceptance of species as a static concept and not as a

dynamic process, given that speciation is a long and complex process. Speciation involves

the establishment of many reproductive barriers and as long as they are incomplete,

hybridization processes may occur. Thus, the establishment of the boundaries delimiting

taxonomic species will be in some cases an arbitrary decision with no evolutionary rele-

vance. However (and to avoid over-complicating this already thorny issue), henceforth I

am going to consider natural hybridization as the gene flow between clearly differentiated

taxa, leaving aside the question as to whether they should be treated as species or

subspecies.

Natural hybridization is a rare process in terms of the total number of individuals that

hybridize, but is not so rare when we look at the number of species that actually hybridize

(Mallet 2005). Hybridization influences the evolutionary trajectory of around 25% of plant

species and 10% of animal species, above all young, recently diverged species (Arnold

1997). Thus, natural hybridization may be an important process in shaping the evolutionary

trajectories of many plants and animals (Eckenwalder 1984; Grant and Grant 1992;

Dowling and DeMarais 1993; Arnold 1997; Rieseberg et al. 2003; Seehausen 2004).

Interestingly, among vertebrates, these processes seem to be most frequent in birds (Grant

and Grant 1992), where speciation usually involves low genetic differentiation and where

post-mating barriers seem to evolve more slowly than in other vertebrates (Prager and

Wilson 1975; Fitzpatrick 2004).

The consequences of hybridization

Natural hybridization can either promote evolutionary divergence between taxa, for

example by reinforcement (Servedio 2004; Hoskin et al. 2005; Urbanelli and Porretta 2008),

or prevent it (Mayr 1963; Coyne and Orr 2004). Species’ integrity will depend on rates of

dispersal and gene flow between taxa, and natural selection in the species involved and in

the resulting hybrids. Thus many different ecological factors, may be involved in the

process. Hybridization between different taxa may potentially lead to a number of different

situations: the establishment of a stable and localized hybrid zone that does not cause the

disappearance of the original species; the disappearance of one of the two original species;

or even the appearance of a new species, resulting from hybrid speciation (Mallet 2007). For

example, if dispersal were high and there were no natural selection forces at work, the gene

exchange between the two diverging lineages would be high and would reduce genetic

differentiation between lineages, thereby turning them into a single species (Arnold 1997).

Nevertheless, dispersal––once thought of as a fixed trait––is now considered to be flexible

(Clobert et al. 2001). Consequently, particular changes in environmental factors (e.g. in

breeding sites or food availability) may change dispersal rates over time, diminishing or

increasing the gene flow between taxa and influencing the relationship between evolu-

tionary lines. Thus, when two diverging lineages come into contact, as in any evolutionary

process, a lot of factors come into play and each situation should be treated as unique.

1436 Biodivers Conserv (2009) 18:1435–1439

123

Is hybridization a conservation concern?

In light of the above rationale––that is, the acceptance of natural hybridization as natural

phenomenon––the answer to this question should be negative. However, no simple answer

is possible, as humans are commonly either directly or indirectly the main cause of sec-

ondary contacts between species. A good example is the introduction of exotic species,

which adapt to their new habitats and may hybridize with local species (Huxel 1999;

Meldgaard et al. 2007; Muñoz-Fuentes et al. 2007). Another example is of the the

hybridizations occurring due to human-mediated habitat modifications (Wayne and Jenks

1991; Haig et al. 2004). This situation becomes even trickier when one of the species is

endangered (Rhymer and Simberloff 1996; Fredrickson and Hedrick 2006). Consequently,

we should first ask if the hybridization event is due to anthropogenic reasons and, secondly,

if one of the two species involved is endangered. If the answers to these two questions are

both negative, then the course of action to be undertaken is clear: we should just observe

and learn. However, how should we proceed in any of the other cases? In my view,

conservation biologists and managers do have a responsibility to take decisions and their

commitment should depend on the severity of the consequences of the hybridization in

question and on the viability of conservation management strategies. When hybridization is

incipient or restricted (in space or time) and management is thus viable, a heuristic action

would be to cull introduced individuals and the resulting hybrids. This type of management

has been carried out in the case of the White-headed Duck Oxyura leucocephala and the Ruddy Duck O. jamaicensis. The latter species was introduced into Great Britain by humans in the middle of the twentieth century and has spread throughout Europe,

hybridizing with the endangered White-headed Duck (Muñoz-Fuentes et al. 2007). In this

case, even though the eradication of Ruddy Ducks is very difficult, the restricted locali-

zation of the endangered species allows (at least temporally) exotic and hybrid individuals

to be controlled. Another example is the release of foreign trout or salmon species for

recreational fishing on rivers. Although it is quite clear that this can constitute a serious

conservation problem wherever they displace the local species (Ruzycki et al. 2003;

McHugh et al. 2008), some introduced salmonid species do not cross with local species or,

where they do, only produce non-fertile descendents. However, other species are able to

interbreed with local species and produce fertile hybrids (Meldgaard et al. 2007). If

hybridization is not generalized, we can act by controlling exotic individuals and, even

more importantly, by protecting rivers that are free of introduced individuals. When

hybridization is extensive in space and time, efficient management options are very

complex, if not impossible. An example of this is the hybridization of the Pacific Black

Duck Anas superciliosa in New Zealand with the introduced Mallard Anas platyrhynchos. Mallards are much more abundant than Pacific Black Ducks and hybridization is wide-

spread. Management is thus very difficult and the probabilities that the Pacific Black Duck

will become extinct are very high. We should also bear in mind the fact that if management

strategies are to be useful, then the original cause of the hybridization should first be

resolved. For instance, the Spotted Owl Strix occidentalis in northwest America is clearly in regression as a result of the logging of old forests (Haig et al. 2004). On the other hand,

the Barred Owl Strix varia seems not to be affected by this habitat modification and has been expanding westwards. The distribution of the two species now overlaps, thereby

favouring hybridization. In this case, before any other management actions are contem-

plated, habitat modification should be halted and the previous situation of the habitat

should be restored as much as is possible. Only then will it make sense to eliminate Barred

Owls and hybrids within the distribution area of the Spotted Owl. Another example of a

Biodivers Conserv (2009) 18:1435–1439 1437

123

problematic situation in conservation is that of the Balearic Shearwater Puffinus maure- tanicus. This species is critically endangered (Oro et al. 2004) and hybridization with the Yelkouan Shearwater has been detected (Genovart et al. 2007; Genovart et al. submitted).

These authors suggest that the hybridization between these two young species is a natural

evolutionary process and, owing to the highly endangered situation of the Balearic

shearwater, immediate conservation efforts should concentrate on enhancing adult survival

rates in this species––its main conservation problem––and on protecting its breeding areas

as means to reversing the dramatic decline that it is undergoing.

In conclusion, it is impossible to provide managers with a simple handbook that will

explain how to proceed in cases of hybridization: each situation will be different and

should be analyzed on a case-by-case basis. The only advice is that the more we know

about the hybridization process and the ecological factors involved, the more able we will

be to analyse each situation as a means to establishing possible consequences and even

estimating the probability of success of any particular conservation action.

Acknowledgments I am very grateful to J.M. Igual, D. Oro, A. Sanz and G. Tavecchia for providing helpful comments on an earlier version of the manuscript. MG was funded by an I3P postdoctoral fellowship from the Spanish Ministry of Education and Science.

References

Arnold ML (1997) Natural hybridization and evolution, Oxford series in ecology and evolution. Oxford University Press, Oxford

Clobert J, Danchin E, Dhondt AA, Nichols JD (2001) Dispersal. Oxford University Press, Oxford Coyne JA, Orr HA (2004) Speciation. Sinauer and Associates, Sunderland, Massachusetts Dowling TE, DeMarais BD (1993) Evolutionary significance of introgressive hybridization in cyprinid

fishes. Nature 362:44–446. doi:10.1038/362444a0 Eckenwalder JE (1984) Natural intersectional hybridization between North American species of Populus

(Salicaceae) in sections Aigeiros and Tacamahaca I. Population studies of P. X parryi. Can J Bot 62:317–324. doi:10.1139/b84-050

Fitzpatrick BM (2004) Rates of evolution of hybrid unviability in birds and mammals. Evolution Int J Org Evolution 58:1865–1870

Fredrickson RJ, Hedrick PW (2006) Dynamics of hybridization and introgression in red wolves and coyotes. Conserv Biol 20:1272–1283

Futuyama D (1998) Evolutionary biology, 3rd edn. Sinauer Associates, Sunderland, MA Genovart M, Oro D, Juste J, Bertorelle G (2007) What genetics tell us about the conservation of the critically

endangered Balearic Shearwater? Biol Conserv 137:283–293. doi:10.1016/j.biocon.2007.02.016 Genovart M, Oro D, Juste J and Contreras H (submitted). Natural hybridisation between the critically

endangered Balearic shearwater and its sibling species the Yelkouan shearwater. Mol Ecol Grant PR, Grant RB (1992) Hybridization of bird species. Science 256:193–197. doi:10.1126/science.

256.5054.193 Haig SM, Mullins TD, Forsman ED, Trail PW, Wennerberg L (2004) Genetic identification of Spotted Owls,

Barred Owls, and their hybrids: legal implications of hybrid identity. Conserv Biol 18:1347–1357. doi: 10.1111/j.1523-1739.2004.00206.x

Hoskin CJ, Higgie H, McDonald KR, Moritz C (2005) Reinforcement drives rapid allopatric speciation. Nature 437:1353–1356. doi:10.1038/nature04004

Huxel GR (1999) Rapid displacement of native species by invasive species: effects of hybridization. Biol Conserv 89:143–152. doi:10.1016/S0006-3207(98)00153-0

Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237. doi:10.1016/ j.tree.2005.02.010

Mallet J (2007) Hybrid speciation. Nature 466:279–283. doi:10.1038/nature05706 Mayr E (1942) Systematics and the origin of species. Columbia University Press, NY Mayr E (1963) Animal species and evolution. Harvard University Press, Cambridge McHugh P, Budy P, Thiede G, VanDyke E (2008) Trophic relationships of nonnative brown trout, Salmo

trutta, and native Bonneville cutthroat trout, Oncorhynchus clarkii utah, in a northern Utah, USA river. Environ Biol Fishes 81:63–75. doi:10.1007/s10641-006-9171-8

1438 Biodivers Conserv (2009) 18:1435–1439

123

Meldgaard T, Crivelli AJ, Jesensek D, Poizat G, Rubin J-F, Berrebi P (2007) Hybridization mechanisms between the endangered marble trout (Salmo marmoratus) and the brown trout (Salmo trutta) as revealed by in-stream experiments. Biol Conserv 136:602–611. doi:10.1016/j.biocon.2007.01.004

Muñoz-Fuentes V, Vilà C, Green AJ, Negro JJ, Sorenson MD (2007) Hybridization between white-headed ducks and introduced ruddy ducks in Spain. Mol Ecol 16:629–638. doi:10.1111/j.1365-294X.2006. 03170.x

Oro D, Aguilar JS, Igual JM, Louzao M (2004) Modelling demography and extinction risk in the endangered Balearic shearwater. Biol Conserv 116:93–102. doi:10.1016/S0006-3207(03)00180-0

Prager EM, Wilson AC (1975) Slow evolutionary loss of the potential for interspecific hybridization in birds: a manifestation of slow regulatory evolution. Proc Natl Acad Sci USA 72:200–204. doi: 10.1073/pnas.72.1.200

Rhymer JM, Simberloff D (1996) Extinction by hybridization and introgression. Annu Rev Ecol Syst 27:83– 109. doi:10.1146/annurev.ecolsys.27.1.83

Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301:1211–1216. doi:10.1126/science.1086949

Ruzycki JR, Beauchamp DA, Yule DL (2003) Effects of introduced lake trout on native cutthroat trout in Yellowstone Lake. Ecol Appl 13:23–37. doi:10.1890/1051-0761(2003)013[0023:EOILTO]2.0.CO;2

Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207. doi: 10.1016/j.tree.2004.01.003

Servedio MR (2004) The what and why of research on reinforcement. PLoS Biol 2:2032–2035. doi: 10.1371/journal.pbio.0020420

Urbanelli S, Porretta D (2008) Evidence of reinforcement of premating isolation between two species of the genus ochthebius (coleoptera: hydraenidae). Evolution. doi:10.1111/j.1558-5646.2008.00381.x

Wayne RK, Jenks SM (1991) Mitochondrial analysis implying extensive extensive hybridization of the endangered red wolf Canis rufus. Nature 351:565–568. doi:10.1038/351565a0

Biodivers Conserv (2009) 18:1435–1439 1439

123