Reconstructing patterns of reticulate evolution in angiosperms

12 Pages·2006·0.59 MB·English

54 (3) • August 2005: 593–604 Vriesendorp & Bakker •Reconstructing reticulate evolution
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NEW TRENDS IN PLANT SYSTEMATICS
edited by Daniel Crawford & Mark E. Mort
Reconstructing patterns of reticulate evolution in angiosperms: what can we
do?
Bastiaantje Vriesendorp & Freek T. Bakker
Nationaal Herbarium Nederland, Wageningen University branch, and Biosystematics Group, Wageningen UR;
Generaal Foulkesweg 37, 6703 BLWageningen, The Netherlands. [email protected] (author for
correspondence); [email protected]
Hybridization is thought to be an important phenom- patterns, and plant species-level relationships are pre-
enon in angiosperm evolution, and it has been suggested dominantly depicted as trees. The question can be asked
that a majority of all plant species may be derived from whether this is because there are no suitable tools avail-
past hybridization events (e.g., Stebbins, 1959; Raven, able for detection or whether the problem is merely
1976; Grant, 1981; Arnold, 1997). In addition, there is an ignored. In this paper we will explore the current practice
increasing interest in the reconstruction of reticulate pat- of dealing with hybrid terminals in published phyloge-
terns (e.g., Linder & Rieseberg, 2004), with increased netic studies, briefly describe a selection of network-pro-
emphasis on the need to explore multiple independent ducing methods currently available, as well as discuss
markers to investigate the origin of putative hybrid future possibilities of reconstructing reticulate patterns in
species (e.g., Hamzeh & Dayanandan, 2004; Koontz & angiosperm evolution.
al., 2004 and other examples listed in Table 1). Several Many recently published studies report the occur-
reviews have recently been published on the process of rence of plant hybrids in several plant genera and fami-
hybridization itself or on issues indirectly related to it: lies, both at the polyploid and homoploid level (e.g.,
Hegarty & Hiscock (2005) and Zhou & al. (2005) present Spartina [Poaceae] in Ainouche & al., 2004; Actinidia
an overview of molecular techniques as well as criteria [Actinidiaceae] in Chat & al., 2004; Glycine [Fabaceae]
for distinguishing hybrid speciation; Gross & Rieseberg in Doyle & al., 2004; Phoenix[Arecaceae] in Gonzalez-
(2005) evaluate the ecological genetics of homoploid Perez & al., 2004; Pleione [Orchidaceae] in Gravendeel
hybrid speciation, and Seehausen (2004) reviewed the & al., 2004; Gagea[Liliaceae] in Peterson & al., 2004).
possible role of hybridization in adaptive radiation. Ellstrand & al. (1996) surveyed frequency and taxonom-
Mallet (2005) presented several hybrid examples in ic distribution of spontaneous hybridization in vascular
plants and animals to discuss the evolutionary signifi- plants in five major floras. They concluded that most
cance of hybridization. Also, many studies have been hybrids are concentrated in particular families such as
published in the past several years on the incidence and Poaceae, Cyperaceae and Rosaceae, and several genera
role of (allo)polyploidy in evolution (e.g., in Soltis & within these families account for most of the hybrid
Soltis, 1993, 2000; Ramsey & Schemske, 1998; Otto & species encountered (Ellstrand & al., 1996). Some life-
Whitton, 2000; Crawford & Mort, 2003; Soltis & al., history characteristics seemed to be associated with
2004). hybridizing taxa such as perennial habit, asexual repro-
In addition to species-level hybridization, other ductive modes, and outcrossing breeding system
(genome-level or molecular) evolutionary processes such (Ellstrand & al., 1996; Rieseberg, 1997; Wisseman &
as recombination, gene conversion or horizontal gene Ritz, 2005). However, it is unclear whether the observed
transfer can confound the phylogenetic signal in the data uneven distribution is due to intrinsic (biological) differ-
to such an extent that it may become non-treelike, and ences of the lineages involved (such as breeding system
phylogenetic methods are not appropriate for analysis. It or ecological preferences), or to extrinsic factors such as
is best to check prior to phylogenetic analysis whether extreme habitat or ecological transitions (Rieseberg,
this applies, and if so, then use network methods to rep- 1997; Gross & Rieseberg, 2005), or distribution pattern
resent it (Bryant & Moulton, 2004). (the extent of sympatry with other species). Also, sam-
Nevertheless, the pages of botanical systematic jour- pling bias could be a factor with the number of reports on
nals are still remarkably devoid of examples of reticulate hybrids influenced by the systematic attention given to
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Vriesendorp & Bakker •Reconstructing reticulate evolution 54 (3) • August 2005: 593–604
Table 1. List of representative phylogenetic studies in angiosperms which include putative hybrids.
Ploidy level External
Species/ of putative evidence on
Genus References acc.1 hybrid Markers used hybrid status2
Achillea Guo & al., 2004 63/82 polyploid nrDNAITS; cpDNAtrnL-F morph; AFLP
Actinidia Chat & al., 2004 40/79 mix mtDNAnad; cpDNAmatK, psbC-trnS, -
rbcL, trnL-F
Amelanchier Campbell & al., 1997 19/26 polyploid nrDNAITS morph; pl
Anacamptis Bateman & Hollingsworth, 3/4 diploid? morphology; nrDNAITS; cpDNA geo
2004 trnL-F; RFLP
Arabis Koch & al., 2003 3/402 triploid nrDNAITS; chromosome counts morph
Armeria Aguilar & Feliner, 2003 72/131 diploid nrDNAITS morph; geo; DNA
Calopogon Goldman & al., 2004 5/56 polyploid cpDNArestriction analysis; nrDNA -
ITS, AFLP; chromosome counts
Cardamine Marhold & al., 2004 17/36 diploid nrDNAITS; AFLP -
Cardamine Lihova & al., 2004 22/22 tetraploid nrDNAITS; cpDNAtrnL-F pl
Ceanothus Hardig & al., 2002 4/23 diploid nrDNAITS; cpDNAmatK; allozymes; morph
morphology
Cicer Shan & al., 2005 9/146 diploid AFLP morph
Dactylorhiza Shipunov & al., 2004 9/125 mix cpDNAtrnL-F, trnS-G, nrDNAITS; -
morphology
Delphinium Koontz & al., 2004 30/30 diploid nrDNAITS; cpDNAtrnL-F morph; cross
DendrochilumBarkman & Simpson, 2002 22/22 mix nrDNAITS; cpDNAaccD morph; geo
Elymus Mason-Gamer, 2004 33/45 hexaploid cpDNArpoA, trnT-L; nDNAGBSSI pl
Elymus Helfgott & Mason-Gamer, 2004 27/27 tetraploid nDNApepC iso
Erythronium Allen & al., 2003 24/24 tetraploid nrDNAITS; cpDNAmatK morph; iso
Fagopyrum Nishimoto & al., 2003 15/15 tetraploid nDNAFlo/Lfy, AG; cpDNArbcL- -
accD, trnK, trnC-rpoB
Gagea Peterson & al., 2004 7/32 diploid? cpDNApsbA-trnH& trnL-F; nrDNA morph
ITS; morphology
Gossypium Cronn & al., 2003 13/13 diploid cpDNAndhF, matK, rpl16, trnL-F; morph; cross
nrDNAITS; nDNACesA1a, AdhC,
CesA1b, A1341, G1121, G1262
Hippophae Sun & al., 2002 15/15 diploid nrDNAITS morph; geo; DNA
Hordeum Petersen & Seberg, 2004 28/30 tetraploid nrDNADMC1, EF-G; cpDNArbcL pl; iso
Lepidium Mummenhoff & al., 2004 56/56 polyploid cpDNAtrnT-L, trnL-F; nrDNAITS morph
Mimulus Beardsley & al., 2004 18/18 diploid? nrDNAITS, ETS; cpDNAtrnL-F morph
Miscanthus Hodkinson & al., 2002 3/5 triploid nrDNAITS; AFLP; cpDNA; FISH pl
Mitella Okuyama & al., 2005 12/66 diploid3 nrDNAITS & ETS; cpDNAmatK, trnL-F-
Nicotiana Chase & al., 2003 66/70 polyploid nrDNAITS; GISH; cpDNAmatK pl, morph
Paeonia Sang & al., 1995 33/45 mix nrDNAITS -
Paeonia Sang & al., 1997 32/37 tetraploid cpDNAmatK; nrDNAITS pl
Paeonia Sang & Zhang, 1999 12/12 tetraploid nDNAAdh1 pl
Pleione Gravendeel & al., 2004 20/20 diploid morphology; nrDNAITS; cpDNA geo
trnT-L, morph; trnL-F, matK
Populus Hamzeh & Dayanandan, 2004 21/21 ? cpDNAtrnL-F; nrDNAITS RFLP
Ranunculus Hörandl & al., 2005 c. 200/ polyploid nrDNAITS morph; pl; cross
200
Sphagnum5 Shaw & al., 2005 31/136 mix nrDNAITS; nDNALeafy/Flo; cpDNA iso
trnL-F; RAPD
Stephanandra Oh & Potter, 2003 9/17 diploid nDNALeafy; nrDNAITS; cpDNA -
trnL-F, trnD-Y-E-T, matK-trnK
Stylosanthes Vanderstappen & al., 2002 28/40 tetraploid STS4; nrDNAITS; cpDNAtrnLintron pl; morph
Tarasa Tate & Simpson, 2003 27/27 polyploid cpDNApsbA-trnH, trnT-L, matK-trnK; -
nrDNAITS
Viburnum Donoghue & al., 2004 42/43 diploid cpDNAtrnK; nrDNAITS geo
Viburnum Winkworth & Donoghue, 2004 41/41 polyploid nDNAGBSSI -
Zaluzianskya Archibald & al., 2005 23/28 ? nrDNAITS; cpDNArpl16, trnL-F -
1Number of ingroup species (including hybrids) /accessions used.
2Evidence is sometimes inferred from the publications, i.e., not stated explicitly by the authors; cross = crossing experiments; DNA= “DNAevidence” (not specified); geo = bio-
geographic distribution; iso = isozymes; morph = morphology; pl = ploidy level.
3Evidence of introgression between taxa; no specific hybrid taxon is identified.
4STS: nuclear sequence-tagged site PCR.
5Bryophyta.
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54 (3) • August 2005: 593–604 Vriesendorp & Bakker •Reconstructing reticulate evolution
particular taxa (Ellstrand & al., 1996). taining the parental species, from 68% to 93% and from
When hybrid species are included in phylogenetic less than 50% to 77%, using AFLP data (Wieringa &
analyses they can affect the overall tree topology. Guhl, in press). The authors argue that this taxon jack-
Remarkably few studies on the behaviour of hybrids in knifing approach could possibly be used as a standard
cladistic analyses have been published. The landmark tool to trace undetected hybrids.
studies of McDade using artificial hybrids of Aphelandra The effect of hybrid exclusion in a combined analy-
(Acanthaceae) are often cited to indicate that a hybrid is sis of nrDNA ITS and chloroplast DNA RFLPs was
not expected to disrupt phylogeny reconstruction unless investigated in Calopogon (Goldman & al., 2004). No
the hybridization event is between divergent lineages effect of removal of the putative hybrid (inferred from its
(McDade, 1990, 1992). However, this is based on a ploidy level) on the combined analyses was found. In
dataset consisting of morphological markers that are contrast, Hoggard & al (2004) studied two tetraploid
mostly intermediate in state for the hybrid, causing it to species of Gaura (Onagraceae) and found a disruptive
be placed at a basal position relative to the most derived effect on tree topology of a putative hybrid with distant
parent. In contrast, molecular characters do not express parents, while no effect was seen for another hybrid with
intermediacy but can display apomorphies of both par- “close” parents.
ents simultaneously (i.e., polymorphic sites or mosaic Cytonuclear incongruencies have confirmed several
sequences) that may cause the hybrid to be placed prox- hypotheses of suspected hybrids, for example,
imate to the most derived parent. Many such apomorphic Anacamptis(Orchidaceae) by Bateman & Hollingsworth
characters shared between hybrid and parents could (2004); Delphinium (Ranunculaceae) by Koontz & al.
cause long-branch attraction (McDade, 1995). (2004); and Dendrochilum(Orchidaceae) by Barkman &
Biparentally-inherited markers expressing additivity will Simpson (2002). Comparison of discordant phylogenetic
possibly influence tree topology (loss of resolution), tree trees from independent datasets has even revealed new
length (increase or decrease depending on treating addi- unexpected cases of possible hybridization (e.g., Braya
tivity as polymorphism or uncertainty, respectively; see [Brassicaceae], Warwick & al., 2004; Stephanandra
Kornet & Turner, 1999), or support analysis (Simmons, [Rosaceae], Oh & Potter, 2003; and Viburnum
2001). Many molecular phylogenetic studies use multi- [Adoxaceae], Donoghue & al., 2004). In addition, this
ple markers with different modes of inheritance (i.e., approach appears promising in phylogeography (see
nuclear and organelle). In fact, Seehausen (2004) uses Comes & Abbott, 2001; Franzke & al., 2004; Lorenz-
the ensuing “cytonuclear discordance” as evidence for Lemke & al., 2005).
ancestral hybridization preceding evolutionary radiation. Of course, incongruent phylogenetic patterns within
Phylogenetic studies are sometimes conducted a dataset or between datasets can have causes other than
excluding putative hybrids in order to avoid (a priori) the hybrid origin of one or more of the species involved.
expected disruptive effects on the analyses (e.g., Such causes may include incomplete lineage sorting, that
Cardamine [Brassicaceae], Marhold & al., 2004 and is, the persistence and retention of ancestral polymor-
Calopogon[Orchidaceae], Goldman & al., 2004) or after phisms through multiple speciation events (e.g., Avise,
determination of incongruence between different gene 2000; Comes & Abbott, 2001; Andreasen & Baldwin,
datasets (e.g., Gaura[Onagraceae], Hoggard & al., 2004 2003; Goldman & al., 2004), homoplasy and taxonomic
and Pleione [Orchidaceae], Gravendeel & al., 2004). In sampling error (Wendel & Doyle, 1998). Therefore,
addition, several authors have analysed their data both hybridization should not be a “standard” interpretation
including and excluding the putative hybrid, in order to when incongruencies are found. Other causes should be
investigate its influence on phylogenetic reconstruction. considered carefully because the incongruent pattern
The effects of hybrid exclusion from nrDNAITS datasets alone can never be an indicator of hybrid status.
was investigated in Achillea (Asteraceae) by Guo & al., Many examples of hybrid detection involve investi-
2004; Armeria (Plumbaginaceae) by Aguilar & Feliner gation of the additivity of nucleotides at single positions
(2003); Delphinium (Ranunculaceae) by Koontz & al. (polymorphic sites) of rDNAITS sequences (e.g., Sun &
(2004); Hippophae (Asteraceae) by Sun & al. (2002); al., 2003; Gravendeel & al., 2004; Koontz & al., 2004;
and Nicotiana (Solanaceae) by Chase & al. (2003). Marhold & al., 2004; Peterson & al., 2004; Warwick &
While the Delphiniumand Nicotianastudies recorded lit- al., 2004). An example of intraspecific ITS additivity can
tle effect of hybrid exclusion on the analysis, the Armeria be found in Clausia aprica (Brassicaceae) where acces-
and Hippophae studies found fewer most parsimonious sions of an intermediate group showed additivity, possi-
trees with a higher consistency index and a higher reso- bly indicating hybridization (Franzke & al., 2004).
lution in the analysis upon hybrid exclusion. In Bikinia Furthermore, hybrid origin and relationship to puta-
(Fabaceae) exclusion of a putative hybrid caused an tive parents, when not extinct, can be explored in more
increase in jackknife support values for both clades con- detail using several different markers. Morphology or
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Vriesendorp & Bakker •Reconstructing reticulate evolution 54 (3) • August 2005: 593–604
patterns of geographical distribution can provide valu- Even more extensive studies have been performed in
able additional evidence for a hybrid origin (Hughes & sunflower hybrid species, where the genomic structure of
Harris, 1998; Bateman & Hollingsworth, 2004; Peterson a newly formed hybrid was compared with that of
& al., 2004; Shan & al., 2005). Additionally, karyologi- ancient hybrids to study the process of diploid hybrid
cal evidence, such as chromosome counts, C-values, and speciation in Helianthus(Rieseberg & al., 1996). In later
GISH or FISH patterns can discriminate between studies, adaptive quantitative trait loci (QTL) were com-
parental genome donors and the hybrid relationships pared to investigate ecological divergence and adaptive
(Hodkinson & al., 2002; Borgen & al., 2003; Chase & genetic variation of the hybrids (Rieseberg & al., 2003;
al., 2003; Bures & al., 2004; Harper & al. 2004; Pires & Lexer & al., 2004). While such genomic evidence can be
al., 2004; Tel-Zur & al., 2004). Another line of evidence regarded as the best and most direct evidence for docu-
for hybrid status can be found using analyses of frag- menting the hybrid nature of a species, as well as allow-
ment-length polymorphisms (e.g., RFLP) or the current- ing assessment of the actual mechanisms involved, such
ly more often employed PCR-based markers (e.g., AFLP, data will probably never be available for most groups on
ISSR, RAPD, or PCR-RFLP). For example, an additive a routine basis.
pattern of AFLPs and the lack of unique bands confirmed
the hybrid status of a species of Mangifera (Teo & al.,
2002). Kiew & al. (2003) used AFLPdata to test hybrid
HYBRID DEFINITIONS
origin in several taxa (Begonia, Mangifera, Nepenthes
and Lausium) and these data permitted the reconstruction The range of possible characteristic hybrid patterns
of relations with the putative parents. Despite many listed above (e.g., additivity of AFLP bands, polymor-
examples where AFLPdata are considered useful in phy- phic nucleotides, incongruence between gene trees, inter-
logenetic studies (e.g., Kardolus & al., 1998; El-Rabey & mediate morphology, etc.), may well not apply to each
al., 2002; Spooner & al., 2005), the application of these hybrid plant species as not all will “behave” in the same
data (and similar single-locus markers) in infrageneric way. Rieseberg & Ellstrand (1993) investigated chemi-
studies requires caution. One major concern involves the cal, morphological and molecular characters in hybrid
difficulty in assessing homology between the co-migrat- plants and found that hybrids can display a range of char-
ing fragments of more distant taxa (El-Rabey & al., acteristics at both the morphological and molecular level.
2002; but see Crawford & Mort, 2004). Therefore, the This ranges from closely resembling one parent to com-
general value of the use of these markers in assessing plete intermediacy between the parentals, and in some
hybrid origin remains questionable as only the successful cases to the formation of a completely new character.
cases tend to get published (but see Krauss & Hopper, The authors emphasised the unpredictable nature of char-
2001, who report that high genetic variability made it dif- acter expression in hybrids, hence preventing hybrid
ficult to distinguish between different hybrid scenarios). detection based on a specific “hybrid character syn-
More insight is needed into the “behaviour” of AFLPs, drome”. Many other studies corroborate these findings
and to this end, simulation (in silicoAFLP, see Koopman with different character patterns found in different
& Gort, 2004) may become increasingly important as hybrids (Table 1). To our knowledge, no recent review on
more complete genome sequences become available patterns in hybrid characters has been performed, com-
(Antonov, 2002). Recent studies of hybrids in parable to the list of Rieseberg & Ellstrand (1993).
angiosperm phylogenies are listed in Table 1, with the The other reason that no general pattern in hybrids
different hybrid detection markers used. can be inferred from published studies lies in inconsis-
Ideally, additional studies, such as crossing experi- tent terminology. For example, Rieseberg and Ellstrand
ments, need to be conducted to support any hybrid (1993) discriminate between “first generation hybrids”,
hypothesis. Artificial crossing experiments permit inves- “later generation hybrids” and “hybrid species”.
tigating the possibility of crossing of the putative parents, According to the authors, the latter category is the most
and also comparison of the character pattern (either difficult to detect, since hybrid species are more prone to
molecular or morphological) in progeny of controlled display many new and extreme characters, while F
1
crosses with that of putative hybrids. For instance, exper- hybrids will probably more often show a blend of char-
imental crosses have been used to investigate morpholo- acters of the parental species. McDade (1995) reviewed
gy and fertility in Solanum (Clausen & Spooner, 1998); character patterns in hybrids and introduced the terms
to compare nrDNAITS sequences between artificial and “primary hybrids” (“with simple histories and little
natural hybrids in Begonia (Chiang & al., 2001); to change since origination”) and “derived hybrids” (with
determine the maternal donor of F hybrids in Phlox “considerable evolutionary change since origination”).
1
(Ferguson & al., 1999); and to study genomic changes in She used these categories to indicate that the amount of
synthetic polyploids of Brassica (Song & al., 1995). evolutionary change will probably define whether
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54 (3) • August 2005: 593–604 Vriesendorp & Bakker •Reconstructing reticulate evolution
hybrids can be dealt with in systematics. “Primary tual framework in which various hybrid definitions are
hybrids” are the only category where we can expect to logically arranged according to factors and scales that are
understand the behaviour of their characters (McDade, of importance in hybrid formation, and hence in charac-
1995). ter evolution (Fig. 1). The two main axes here are “age of
Additionally, the term “hybrid” is used for a wide the hybrid” (whether it is a newly formed (F ) hybrid or
1
variety of entities (McDade, 1995), often without refer- a more ancient and established hybrid species), and the
ence to important factors that must be considered, such taxonomic level of the hybrid’s parents. The latter is fur-
as age, ploidal level and parental phylogenetic distance. ther subdivided into relevant mechanism(s) involved
Most systematic studies dealing with hybrids do not during or after the process of hybridization, such as the
explicitly state what hybrid definition is used, but simply amount of introgression and change in ploidy level. As
assume that a hybrid is a cross between different species, McDade (1995) noted, the pattern of character state
or define it as “interspecific” or “hybrid between transmissions in hybrids and the amount of evolutionary
species”. There are, however, some studies that explicit- change in characters are important for possible detection
ly refer to the age of the hybrid or “stability” of the and behaviour of hybrid terminals in phylogenetic stud-
hybrid individuals. For example Bures & al. (2004) spec- ies. Therefore, we include these factors here as well, and
ify that they include (sterile) F hybrids in their study of nest them within the different time scales.
1
Cirsium; Koontz & al (2001) and Goldman & al. (2004)
both discuss the possibility of ancient hybridization in
respectively Delphinium and Calopogon, but these are
REPRESENTING HYBRIDS IN PHY-
exceptions.
LOGENETIC ANALYSIS: VISUALISA-
The term “hybridization” is rarely specified, instead
TION OF PATTERNS
it is assumed that every worker knows what is meant, but
it is important to note that several definitions exist. The As mentioned above, hybrids are sometimes exclud-
most often used one is by Harrison (1993): “interbreed- ed from phylogenetic analyses, often after incongruence
ing of individuals from two populations, or groups of testing among multiple datasets, or because the hybrid is
populations, which are distinguishable on the basis of expected to have a disruptive effect on the tree topology
one or more heritable characters”. This definition does (e.g., Marhold & al., 2004). This approach intuitively
not require any consideration of species concepts, but makes sense because trees cannot depict hybrids and tree
most workers use the “standard” definition of a hybrid reconstruction could be confounded by their inclusion,
“resulting from crossing between different species”. In with a polytomy a likely result (but see below).
an attempt to clarify matters, we include here a concep- Moreover, when using packages such as Mesquite
Time → F1 Later generation Hybrid species1
Tax. Character expression Close to Inter- Close to Inter- Hybrid aut- Close to Inter- Hybrid aut- Mix/Multiple
Level↓ one mediate2 one parent mediate2 apomorphs3 one parent mediate2 apomorphs3 origins??
parent
Intrasp.4 -- --
homoploid a a a a Deriv ed hybarid sensu McDa,abde 199 5 a,b a a
without
subsequent allopolyploid b b
introgression
Primary hybrid Primary hybrid Primary hybrid Hybrid species
asexual/ sensu sensu McDade 1995 sensu McDa de, 1995 sensu Grant ,1981
other Rieseberg &
Inter- Ellstrand, 1993
specific homoploid c c c c,d c,d
c c c,d c,d
Derived hybrid sensu McDade, 1995
with introgression allopolyploid d d
d d
Primary hybrid sensu Primary hybrid
asexual/ McDade, 1995 sensu McDa de, 1995
other
Supersp.4 -- --
1Stabilised lineage/ancient hybrid.
2Can be either mosaic or additive characters. aHelianthus(Rieseberg & al., 1996, 2003).
3‘New’ characters. bPaeonia (Sang & al., 1995) .
4Does not apply as intra- and superspecific hybridization falls outside cIris (Arnold, 1993, 1997; Arnold & al., 1990, 1991).
standard hybrid terminolog y. dGossypium (Wendel & al., 1991, 1995a,b; Cronn&al., 2 003 ).
Fig. 1. How to become a hybrid? Conceptual framework of commonly-used hybrid terminology with exemplar studies
indicated.
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Vriesendorp & Bakker •Reconstructing reticulate evolution 54 (3) • August 2005: 593–604
(Maddison & Maddison, 2004) or MacClade (Maddison Probably the best way of distinguishing between the
& Maddison, 2005) for optimisation of characters, different above-mentioned causes for the observed phy-
resolved trees are usually required as input. However, it logenetic incongruences is therefore to use additional
would be a waste of potentially important information if data or evidence of hybridization from other sources
the hybrid sequences were not used in such analyses. In such as morphology, genomics and karyology. Yet, in
addition, inclusion of the hybrid might not have a dis- spite of the objections outlined above, a network can be
ruptive effect on the trees after all (see Chase & al., 2003; used as a starting point for investigating relationships.
Guo & al., 2004; Koontz & al., 2004). Whether or not hybridization is the cause, it is desirable
As outlined above, one solution to this problem to display the source of conflict. One way to do this is to
could be to conduct analyses that both include and visualise the character incongruences in a network,
exclude putative hybrids and present both results (as in where a “hybrid” or “problematic terminal” can be con-
Sun & al., 2002; Aguilar & Feliner, 2003; Chase & al., nected to more than one other terminal or internode.
2003; Guo & al., 2004; Koontz & al., 2004; Wieringa & Unfortunately, although some programs exist that
Guhl, in press). An alternative, and perhaps better can deal with population-level data and possibly
approach might be to represent hybrid relationships hybridization events (see below), no method is available
directly in a network. This can be done by hand for rela- that can be considered the perfect “hybrid interpreter”.
tively clear hybrid relationships (Sang & al., 1995; The only way to make progress with this problem is to
Hardig & al., 2002). However, for more complex situa- seek methods to deal with complex hybrid terminals
tions this is not feasible and depicting reticulate evolu- using simulation and experimental data. The common
tionary patterns (and all possible relationships) in one practice of leaving suspected taxa out of the analysis to
network would be a desirable feature in a computer pack- avoid confounding effects on phylogenetic reconstruc-
age. tion will not stimulate further progress. Below we
In analogy to the gene tree/species tree problem explore some of the methods currently available and
(Maddison, 1997), however, the question must be infer possible solutions and suggest some future research
addressed of what is actually represented in such reticu- directions.
lated networks: character conflict or relationships among
organisms (or species)? For instance, Bryant & Moulton
(2002) characterise networks as “a representation of the
data rather than a phylogenetic inference”, and to “indi-
CURRENT TOOLS FOR REPRE-
cate whether or not the data is substantially treelike”.
SENTING INCONGRUENT PHYLO-
Holland & al. (2005), on the other hand, describe their
GENETIC PATTERNS SIMULTANE-
Consensus Network (see below) method as one “that
OUSLY
generalizes the notion of consensus trees to allow con-
flicting evolutionary hypotheses to be displayed within a Posada & Crandall (2001a) listed a range of methods
network”. and software for network estimation that can possibly
While one would certainly like to distinguish “take into account population-level phenomena and
between sources of phylogenetic tree incongruence, it is allow for persistent ancestral nodes, multifurcations and
unlikely that the cause of the conflict can be inferred by reticulations”. Examples are the method of statistical par-
analysing the pattern alone. Both homoplasy/sampling simony (as implemented in the package TCS, Clement &
artifacts and hybridization (or other evolutionary al., 2000), SplitsTree (Huson & Bryant, 2004), and
processes) can give the same (sometimes incongruent) Network (Bandelt & al., 1995, 1999) but so far, these
patterns. Also, hybridization need not necessarily result methods have not been used frequently in published
in a clear reticulated pattern of evolution. The data can studies of angiosperm species phylogenies. In Table 2 we
not indicate any incongruence, for instance, when using list currently available and accessible methods aiming at
uniparentally inherited markers or markers that show network reconstruction. Some of these programs are
strong gene conversion. In addition, processes during or character-based, such as the Median Network and
after hybridization (such as repeated secondary contact, Median-Joining network approach of Bandelt & al.
as for instance under a post-glacial refugium expansion (1995, 1999), but most other methods are distance based.
scenario), can make the actual split “messy”, and hence Generally, programs can be distinguished by whether
the relationships more complex and difficult to resolve. they are based on an algorithmic approach or use an opti-
Nevertheless, Seehausen (2004) argues that “adaptive mality criterion. Most network methods are based on an
radiation” (or at least “functional diversification”) can be algorithmic approach and do not explore alternative solu-
facilitated by interspecific hybridization and that such tions. However, the Median Network approach displays
patterns can be clearly reconstructed. all parsimonious solutions in one network, and it is not
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54 (3) • August 2005: 593–604 Vriesendorp & Bakker •Reconstructing reticulate evolution
Table 2. List of selected currently available network reconstruction packages.
Network reconstruction
Package Reference method Input data Website
Network Bandelt & al., 1995 Median networks1 Binary characters http://www.fluxus-technology.com/
Median-joining networks2 Multistate characters
Spectronet Huber & al., 2002 Median networks1 Binary characters http://awcmee.massey.ac.nz/spectronet/
index.html
Arlequin Schneider & al., 2000 Molecular-variance parsimony3 Multistate characters/ http://lgb.unige.ch/arlequin/
haplotype frequencies
SplitsTree Huson & Bryant, 2004 Split decomposition4 Multistate characters http://www-ab.informatik.uni-tuebingen
or distancesa .de/software/jsplits/welcome.html
NeighborNet5 Multistate characters
or distancesa
Consensus networks6 Treesb
T-rex Makarenkov, 2001 Reticulogram reconstruction7 Distances http://www.labunix.uqam.ca/~makarenv/
trex.html
TCS Clement & al., 2000 Statistical parsimony8 Multistate characters/ http://darwin.uvigo.es/software/tcs.html
haplotype frequencies
aInput data are multistate characters or distances; analysis is based on distances. bInput data are trees; analysis is based on splits of these trees.
1Bandelt & al., 1995. 2Bandelt & al., 1999. 3Excoffier & Smouse, 1994. 4Bandelt & Dress, 1992. 5Bryant & Moulton, 2002, 2004. 6Holland & Moulton, 2003. 7Makarenkov
& Legendre, 2004. 8Templeton & al., 1992.
immediately clear whether an algorithm or criterion- multiple alignments. One of these methods works by
based approach applies here. sliding a window along a sequence alignment, and meas-
Most of the programs listed in Posada and Crandall uring the discrepancy between the trees suggested by the
(2001a) aim at population-level data and there are sever- first and second halves of the window, using distance
al recent examples of their application. For example, matrix methods. If we could use these programs to “cor-
multiple origins in Glycine tomentellawere investigated rect” phylogenetic data sets prior to phylogenetic analy-
by Rauscher & al. (2004) using TCS; representation of sis by scanning and removing recombined regions, this
phylogeographic relationships in dolphins was recon- could prove highly useful.
structed using TCS, Network, Arlequin and SplitsTree Ideally, one would like to test the performance of
(Cassens & al., 2003); and patterns of genetic diversity network reconstruction methods using simulated data as
were explored in Scaevola plumieri (Asteraceae) using has been done for several other phylogenetic methods
SplitsTree (Barker & al., 2003). However, there are few (e.g., Suzuki & al., 2002; Douady & al., 2003; Hall,
examples of applications of using network programs at 2005). However, since many network reconstruction pro-
the angiosperm species-level. For instance, hybrid rela- grams do not have a batch mode, simulation can become
tionships in Opuntia were investigated with the Median a cumbersome enterprise (pers. obs. and L. Nakhleh,
Network approach of Spectronet (Griffith, 2003), and pers. comm.). More importantly, in network simulations
split decomposition (with the program SplitsTree) was it is not clear what test statistic to use when comparing
used to study species radiation and reticulate relation- networks to a simulated model network. Measurements
ships in Ranunculus (Lockhart & al., 2001; Hörandl & such as the partition metric (Robinson & Foulds, 1981)
al., 2005). Also, Median-Joining networks (Bandelt & as used in many simulation studies (e.g., Leitner & al.,
al., 1999) have been used for detailed analyses of intro- 1996; Zwickl & Hillis, 2002; Piontkivska, 2004), are not
gression and hybridization zones between two species of available for a network. Nakhleh & al. (2003) tested the
Populus (Lexer & al., 2005) and Passiflora (Lorenz- performance of SpNet and SplitsTree, using a modified
Lemke & al., 2005). version of the Robinson-Fould metric specifically
In addition to the methods outlined above, there are designed and implemented for their experiments, but not
several methods aimed specifically at detecting recombi- suitable for wider use.
nation (reviewed by Posada & Crandall, 2001b, 2002; In another study, we will focus on the performance
Posada & al., 2002; Posada, 2002). These methods can of selected network reconstruction methods using “real”
only be used to test whether or not recombination is like- published data (Vriesendorp & Bakker, in prep.). Here,
ly to be present in the data and do not display reticulate we would like to note that despite the wealth of examples
relationships. For instance, the new package TOPALi of hybrids in phylogenetic studies (Table 1), the success-
(see http://www.bioss.ac.uk/~iainm/topali/; Milne & al., ful use of network reconstruction seems to be restricted
2004) is one of the available recombination detection to the population level. This is understandable since phy-
programs that has several methods implemented to auto- logenetic DNA sequence datasets usually contain far
matically identify recombinant sequences within DNA higher levels of variation than what most methods are
599
Vriesendorp & Bakker •Reconstructing reticulate evolution 54 (3) • August 2005: 593–604
(Scrophulariaceae s.s., tribe Manuleeae): classification
designed to deal with. Moreover, the consistency and rel-
based on DNA sequences from multiple genomes and
ative performance of these methods at the species level is
implications for character evolution and biogeography.
not well understood, as outlined above. Syst. Bot.30: 196–215.
In conclusion, the question remains whether a net- Arnold, M. L. 1993. Iris nelsonii (Iridaceae) — Origin and
work representation can give a meaningful representa- genetic composition of a homoploid hybrid species. Amer.
tion of species relationships, and whether such an analy- J. Bot.80: 577–583.
Arnold, M. L. 1997. Natural Hybridization and Evolution.
sis provides added value with respect to tree analysis. It
Oxford Univ. Press, Oxford.
remains to be seen whether network representation can
Arnold, M. L., Buckner, C. M. & Robinson, J. J. 1991.
be a good alternative to placement of the hybrid by hand
Pollen-mediated introgression and hybrid speciation in
on a phylogenetic tree (e.g., Sang & al., 1995; Louisiana irises. Proc. Natl. Acad. Sci. U.S.A. 88:
Whitehouse, 2002). However, when networks are not 1398–1402.
interpreted as displaying evolutionary relationships, but Arnold, M. L., Hamrick, J. L. & Bennett, B. D. 1990.
instead represent character conflict in the data, these Allozyme variation in Louisiana irises — a test for intro-
gression and hybrid speciation. Heredity65: 297–306.
packages prove very useful. For instance, uncovering
Avise, J. C. 2000. Phylogeography: The History and
data ambiguity using NeighborNet or Consensus net-
Formation of Species. Harvard Univ. Press, Cambridge,
works in a way that (consensus) trees cannot, is a valu-
Massachusetts.
able addition to our phylogenetic tool palette, providing Bandelt, H. J. & Dress, A.1992. Split decomposition: a new
new insights in the analysis of data structure. and useful approach to phylogenetic analysis of distance
Many network reconstruction methods are based on data. Molec. Phyl. Evol. 1: 242–252.
a combined approach and explore incongruencies within Bandelt, H. J., Forster, P. & Rohl, A.1999. Median-joining
networks for inferring intraspecific phylogenies. Molec.
a combined dataset (Posada & Crandall, 2001a; Linder &
Biol. Evol. 16: 37–48.
Rieseberg, 2004). Exploring and summarising separate
Bandelt, H. J., Forster, P., Sykes, B. C. & Richards, M. B.
datasets (or gene trees) could have preference above
1995. Mitochondrial portraits of human-populations using
combining all data “a priori” and conducting simultane- median networks. Genetics141: 743–753.
ous analysis. In their review, Linder & Rieseberg (2004) Barker, N. P., Harman, K. T., Ripley, B. S. & Bond, J.2003.
stress the importance of using multiple independent The genetic diversity of Scaevola plumieri
markers in the reconstruction of patterns of reticulate (Goodeniaceae), an indigenous dune coloniser, as revealed
by Inter Simple Sequence Repeat (ISSR) fingerprinting. S.
evolution in plants. The best approach appears to be to
African J. Bot.68: 532–541.
combine as many independent gene trees as possible into
Barkman, T. J. & Simpson, B. B. 2002. Hybrid origin and
a species tree and infer hybrid relationships from there. A
parentage of Dendrochilum acuiferum (Orchidaceae)
similar approach is proposed by Nakhleh & al. (in press) inferred in a phylogenetic context using nuclear and plas-
in their package RIATA-HGT, which enables inference tid DNAsequence data. Syst. Bot.27: 209–220.
of horizontal gene transfer events based on analysis of Bateman, R. M. & Hollingsworth, P. M. 2004.
incongruence among species and gene trees. Morphological and molecular investigation of the parent-
age and maternity of Anacamptis xalbuferensis (A. fra-
grans ×A. robusta), a new hybrid orchid from Mallorca,
Spain. Taxon53: 43–54.
Beardsley, P. M., Schoenig, S. E., Whittall, J. B. &
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