Molecular Ecology (2010) 19, 5079–5083
NEWS AND VIEWS
PERSPECTIVE
Speciation genetics of biological invasions with hybridization
ROBB T. BRUMFIELD
Museum of Natural Science and Department of Biological
Sciences, Louisiana State University, Baton Rouge, LA 70803,
USA
The negative effects of human-induced habitat disturbance
and modification on multiple dimensions of biological
diversity are well chronicled (Turner 1996; Harding et al.
1998; Lawton et al. 1998; Sakai et al. 2001). Among the more
insidious consequences is secondary contact between formerly allopatric taxa (Anderson & Hubricht 1938; Perry
et al. 2002; Seehausen 2006). How the secondary contact will
play out is unpredictable (Ellstrand et al. 2010), but if the
taxa are not fully reproductively isolated, hybridization is
likely, and if the resulting progeny are fertile, the eventual
outcome is often devastating from a conservation perspective (Rhymer & Simberloff 1996; Wolf et al. 2001; McDonald et al. 2008). In this issue of Molecular Ecology, Steeves
et al. (2010) present an analysis of hybridization between
two avian species, one of which is critically endangered and
the other of which is invasive. Their discovery that the
endangered species has not yet been hybridized to extinction is promising and not what one would necessarily
expect from theory.
Keywords: birds, conservation genetics, hybridization, invasive species, speciation
Received 13 September 2010; revision received 28 September
2010; accepted 28 September 2010
From the point of view of a speciation geneticist, the study
system Steeves et al. (2010) examine is fascinating. Habitat
modification has facilitated the colonization of poaka (also
known as the pied stilt; Himantopus himantopus leucocephalus), a generalist wading bird native to Australia, into New
Zealand, where it has come into secondary contact with
endemic kakı
! (also known as the black stilt; Himantopus novaezelandiae), a braided river specialist (Figs 1, 2 and 3).
The ensuing hybridization between the two stilts provides
a natural laboratory to help understand both the genetics
of speciation and the evolutionary consequences of biological invasions that are accompanied by hybridization (Hewitt 1988). But because kakı
! are one of the world’s most
Correspondence: Robb Brumfield, Fax: 225-578-3075;
E-mail: [email protected]
! 2010 Blackwell Publishing Ltd
endangered birds — only 98 individuals were tabulated in
2010, up from approximately 23 in 1981 — the study system is exceedingly fragile (Bird et al. 2009).
In plants, hybridization has been a major evolutionary
force in the creation of new species through, for example,
allopolyploidy (Grant 1961; Arnold 1997; Rieseberg 1997;
Soltis & Soltis 2000; Vellend et al. 2007). In contrast, speciation via hybridization is thought to occur relatively rarely
in animals (Mallet 2007). From a theoretical perspective,
the most likely effects of hybridization in animals include
everything from relatively low level amounts of introgression in which species boundaries are more or less maintained (Fitzpatrick et al. 2010), to the formation of a hybrid
swarm (a population composed of a diversity of recombinants) (Harrison 1993). Its genome disintegrated, the formation of a hybrid swarm spells the genetic extinction of a
hybridizing species if it has no other parental populations
away from the swarm. Linking this back to Homo sapiens,
human-induced disturbance is considered the most frequent underlying cause of extinction by hybridization
(Seehausen et al. 2008), and, unfortunately, the literature is
now replete with examples of this phenomenon (Rhymer &
Simberloff 1996).
Anecdotally, kakı
! have been long thought by many biologists to already be genetically extinct, the few remnant
individuals simply representing black-plumaged recombinant phenotypes in a hybrid swarm (Fig. 1). This is a reasonable assumption given the theoretical outcomes of
biological invasions that include hybridization in animals
(Fig. 4). Allendorf et al. (2001) identified three general outcomes of anthropogenically induced hybridization, with
the caveat that outcomes in real biological situations exhibit a continuum: (i) hybridization without introgression; (ii)
widespread introgression; and (iii) complete admixture.
Hybridization without introgression usually occurs if
hybridization events are very rare, with any fertile F1s subject to the same stochastic processes that influence the fitness of any individual in a population, or, if hybridization
events are common, because F1s are sterile or suffer greatly
reduced fitness. In the stilts, hybridization has been occurring for at least 50 years (approximately 15 generations),
and breeding data, plus the presence of backcrossed individuals in the population, indicate F1s are fertile and
reproducing. The second possible outcome, widespread
introgression, denotes genetic admixture in and around the
point of hybridization, but with the presence of geographically isolated or distant reservoir parental populations that
are unaffected by hybridization. That the entire kakı
! distribution is found in the Upper Waitaki Basin negates the
gene reservoir concept.
Sadly, for kakı
!, the most probable expected outcome is
extinction of the species through the formation of a hybrid
5080 N E W S A N D V I E W S : P E R S P E C T I V E
(a)
(b)
(c)
(d)
Fig. 2 Map of the Upper Waitaki Basin on the South Island of
New Zealand. Once abundant and widely distributed, kakı
! are
currently restricted to the Upper Waitaki Basin, where its
range overlaps with poaka. Map credit Matt Walters.
swarm, genetic disintegration of its genome and genetic
assimilation into poaka (Fig. 4). In the context of a biological invasion, a hybrid swarm can form rapidly as invading
alleles diffuse from the point of contact into the native species (Kot et al. 1996; Pialek & Barton 1997; Huxel 1999;
Perry et al. 2001; Blum et al. 2010). The swarm is characterized, at least initially, by relatively high levels of nuclear
and cytonuclear disequilibria because of the tendency for
the two co-adapted genomes to have a selective advantage
over hybrids (Nei & Li 1973; Szymura & Barton 1991;
Arnold 1993; Barton & Gale 1993). If the swarm has a continued influx of invading migrants carrying parental, unrecombined genomes into the swarm, it is expected to decay
as a function of migration rate, recombination rate, effective population size and the fitness of hybrids relative to
parentals. With no source of parental native genomes and
a steady stream of parental invasive genomes migrating
into the swarm, genetic drift can lead to the total genetic
Fig. 1 Images of (a) the New Zealand endemic and critically
endangered kakı
! (Himantopus novaezelandiae). (b) a dark recombinant phenotype. The plumage illustrated corresponds to the
G plumage in Fig. 1 of Steeves et al. (2010). (c) a light recombinant phenotype corresponding to the D1D2 plumage. (d) the
invading poaka (H. himantopus leucocephalus). Photograph credits Dave Murray.
! 2010 Blackwell Publishing Ltd
N E W S A N D V I E W S : P E R S P E C T I V E 5081
Fig. 3 Aerial image of the Tasman River in the Upper Waitaki Basin on the South Island of New Zealand. Braided rivers, like the
Tasman River, are characterized by many small channels and small intervening islands. Photograph credits Dave Murray.
loss of the native species unless some neutral or selectively
advantageous alleles persist as assimilated new variation
in the invading species’ genome (Barton 1979; Harrison
1990). There are many cases in which the level of genetic
variation in a hybridizing invasive species increases, and
in some instances this variation can be adaptive (Lee 2002;
Lambrinos 2004; Richards 2005).
Contrary to the expected effects of hybridization on
kakı
!, Steeves et al. (2010) found little evidence of cytoplasmic introgression, and the nuclear introgression uncovered was in the direction from endangered kakı
! into
poaka. In other words, based on genetic variation at the
mitochondrion and eight microsatellite loci, endangered
kakı
! are persisting as a distinct evolutionary unit despite
multiple generations of ‘successful’ hybridization with
poaka. From a species genetic perspective, it is remarkable that species boundaries of these closely related taxa
have been maintained in the face of hybridization.
Here, the discrepancy between the model-based expectation and empirical reality has its explanation in the biological details. The lack of cytoplasmic introgression between
poaka and kakı
! can be explained in part by the dominance
theory of Haldane’s rule (Haldane 1922), which states that
when hybrids show reduced fitness, the effects are stronger
in the heterogametic sex. That females are the heterogamet! 2010 Blackwell Publishing Ltd
ic sex in birds and mitochondrial inheritance is matrilineal
explain the limited mitochondrial introgression in part,
especially since female hybrid stilts are known to suffer
reduced fitness. Ironically, another probable factor in kakı
!
survival is small population size. This contributed to a
transient male-biased sex ratio of kakı
! during the late
1900s, so that most matings were between male kakı
! and
female poaka or hybrids, combinations that are known to
produce offspring of reduced fitness. The small population
size also led to an exceptionally high mortality rate of stilts
during the period in which the two species have been in
contact and hybridizing. Thus, few of the offspring during
the period of hybridization contributed to the current
genetic pool.
The history of kakı
! conservation management is emblematic of the challenges that hybridization presents. In the
case of kakı
!, hybridization was first ignored so as to focus
efforts entirely on the reproductive success of pure-breeding pairs. An allozyme study indicating that dark hybrids
were genetically intermediate led to the equal inclusion of
dark hybrids in conservation efforts, but a subsequent
study that suggested mixed pairs suffer from reduced fitness led to a renewed focus on pure-breeding kakı
!. Despite
this tumultuous management history, the results from the
Steeves et al. study and the increased number of kakı
!
5082 N E W S A N D V I E W S : P E R S P E C T I V E
Secondary contact
Source population
of invasive species
Hybrid swarm
Genetic disintegration of
native species
Source population
of invasive species
Genetic assimilation of
native species
Source population
of invasive species
Genetic variation in Average linkage disequilibria
invasive population
in hybridizing population
Source population
of invasive species
Hybrid swarm
Native species as a
genetic unit is extinct
Time course of biological invasion with hybridization
Fig. 4 (a) A nonequilibrium model of the formation and fate of a hybrid swarm involving an invasive species (white rectangles)
hybridizing with a native species composed of a single small population (black rectangles). The assumptions of the model include
reduced fitness of hybrids relative to parentals, unidirectional migration into the swarm of the invasive species from a parental
source population, and no speciation by hybridization. (b) Because of reduced hybrid fitness, there is selection against disrupting the
co-adapted genomes of the hybridizing species. Combined with the influx of parental invasive genomes into the swarm, there will
be significant nuclear and cytonuclear disequilibria in the swarm. (c) As portions of the native species genome are assimilated, the
amount of genetic variation in the invading species increases and linkage disequilibria decay.
suggest the effort spent on its conservation is working. Still,
it is premature to sound the victory bell. Molecular techniques used today by most conservation geneticists, including those employed by Steeves et al., allow one to sample
only a fraction of the genome. Thus, poaka alleles that have
introgressed into kakı
! may have gone undetected. Addressing that question will require a more comprehensive analysis of the genomic architecture of these hybridizing taxa.
One of the great hopes of next-generation sequencing technologies is that genome-scale sequencing scans will be possible for studies of nonmodel taxa, including those on the
brink of extinction (Lerner & Fleischer 2010).
References
Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends in
Ecology & Evolution, 16, 613–622.
Anderson E, Hubricht L (1938) Hybridization in Tradescantia. III.
The evidence for introgressive hybridization. American Journal of
Botany, 25, 396–402.
Arnold ML (1993) Cytonuclear disequilibria in hybrid zones.
Annual Review of Ecology and Systematics, 24, 521–554.
Arnold ML (1997) Natural Hybridization and Evolution. Oxford University Press, New York.
Barton NH (1979) Gene flow past a cline. Heredity, 43, 333–
339.
Barton NH, Gale KS (1993) Genetic analysis of hybrid zones. In:Hybrid Zones and the Evolutionary Process (ed Harrison RG), pp. 13–
45. Oxford University Press, New York.
Bird J, Butchart S, Symes A (2009) Himantopus novaezelandiae. In:
IUCN Red List of Threatened Species. Version 2010.3. http://
www.iucnredlist.org/apps/redlist/details/144083/0. Downloaded on 21 October 2010.
Blum MJ, Walters DM, Burkhead NM, Freeman BJ, Porter BA
(2010) Reproductive isolation and the expansion of an invasive
hybrid swarm. Biological Invasions, 12, 2825–2836.
! 2010 Blackwell Publishing Ltd
N E W S A N D V I E W S : P E R S P E C T I V E 5083
Ellstrand NC, Biggs D, Kaus A et al. (2010) Got hybridization? A
multidisciplinary approach for informing science policy. BioScience, 60, 384–388.
Fitzpatrick BM, Johnson JR, Kump DK et al. (2010) Rapid spread
of invasive genes into a threatened native species. Proceedings of
the National Academy of Sciences USA, 107, 3606–3610.
Grant V (1961) Plant Speciation. Columbia University Press, New
York.
Haldane JBS (1922) Sex ratio and unisexual sterility in animal
hybrids. Journal of Genetics, 12, 101–109.
Harding JS, Benfield EF, Bolstad PV, Helfman GS, Jones EBD
(1998) Stream biodiversity: the ghost of land use past. Proceedings
of the National Academy of Sciences USA, 95, 14843–14847.
Harrison RG (1990) Hybrid zones: windows on the evolutionary
process. In:Oxford Surveys in Evolutionary Biology (eds Futuyma
D, Antonovics J), pp. 70–114. Oxford University Press, Oxford.
Harrison RG (1993) Hybrids and hybrid zones: historical perspective. In:Hybrid zones and the Evolutionary Process (ed Harrison
RG), pp. 3–12. Oxford University Press, New York.
Hewitt GM (1988) Hybrid zones-natural laboratories for evolutionary studies. Trends in Ecology and Evolution, 3, 158–167.
Huxel GR (1999) Rapid displacement of native species by invasive
species: effects of hybridization. Biological Conservation, 89, 143–
152.
Kot M, Lewis MA, van den Driessche P (1996) Dispersal data and
the spread of invading organisms. Ecology, 77, 2027–2042.
Lambrinos JG (2004) How interactions between ecology and evolution influence contemporary invasion dynamics. Ecology, 85,
2061–2070.
Lawton JH, Bignell DE, Bolton B et al. (1998) Biodiversity inventories, indicator taxa and effects of habitat modification in tropical
forest. Nature, 391, 72–76.
Lee CE (2002) Evolutionary genetics of invasive species. Trends in
Ecology & Evolution, 17, 386–391.
Lerner HRL, Fleischer RC (2010) Prospects for the use of next-generation sequencing methods in ornithology. Auk, 127, 4–15.
Mallet J (2007) Hybrid speciation. Nature, 446, 279–283.
McDonald DB, Parchman TL, Bower MR, Hubert WA, Rahel FJ
(2008) An introduced and a native vertebrate hybridize to form a
genetic bridge to a second native species. Proceedings of the
National Academy of Sciences USA, 105, 10837–10842.
Nei M, Li W-H (1973) Linkage disequilibrium in subdivided populations. Genetics, 75, 213–219.
Perry WL, Feder JL, Dwyer G, Lodge DM (2001) Hybrid zone
dynamics and species replacement between Orconectes cray-
! 2010 Blackwell Publishing Ltd
fishes in a northern Wisconsin Lake. Evolution, 55, 1153–
1166.
Perry WL, Lodge DM, Feder JL (2002) Importance of hybridization
between indigenous and nonindigenous freshwater species: an
overlooked threat to North American biodiversity. Systematic
Biology, 51, 255–275.
Pialek J, Barton NH (1997) The spread of an advantageous allele
across a barrier: the effects of random drift and selection against
heterozygotes. Genetics, 145, 493–504.
Rhymer JM, Simberloff D (1996) Extinction by hybridization and
introgression. Annual Review of Ecology and Systematics, 27, 83–
109.
Richards AJ (2005) Hybridisation – reproductive barriers to gene
flow. In: Gene flow from GM plants, (eds Poppy GM, Wilkinson
MJ), pp. 78–112. Blackwell Publishing, Oxford.
Rieseberg LH (1997) Hybrid origins of plant species. Annual Review
of Ecology and Systematics, 28, 359–389.
Sakai AK, Allendorf FW, Holt JS et al. (2001) The population biology of invasive species. Annual Review of Ecology and Systematics,
32, 305–332.
Seehausen O (2006) Conservation: losing biodiversity by reverse
speciation. Current Biology, 16, R334–R337.
Seehausen O, Takimoto G, Roy D, Jokela J (2008) Speciation reversal and biodiversity dynamics with hybridization in changing
environments. Molecular Ecology, 17, 30–44.
Soltis PS, Soltis DE (2000) The role of genetic and genomic attributes in the success of polyploids. Proceedings of the National
Academy of Sciences USA, 97, 7051–7057.
Steeves TE, Maloney RF, Hale ML, Tylianakis JM, Gemmell NJ
(2010) Genetic analyses reveal hybridization but no hybrid swarm
in one of the world’s rarest birds. Molecular Ecology, 19, 5090–5100.
Szymura J, Barton NH (1991) The genetic structure of the hybrid
zone between the Fire-bellied Toads Bombina bombina and B. variegata: comparisons between transects and between loci. Evolution, 45, 237–261.
Turner IM (1996) Species loss in fragments of tropical rain forest: a
review of the evidence. Journal of Applied Ecology, 33, 200–209.
Vellend M, Harmon LJ, Lockwood JL et al. (2007) Effects of exotic
species on evolutionary diversification. Trends in Ecology & Evolution, 22, 481–488.
Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk
of extinction through hybridization. Conservation Biology, 15,
1039–1053.
doi: 10.1111/j.1365-294X.2010.04896.x