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(American Journal of Botany. 2008;95:1109-1121.) doi: 10.3732/ajb.2007403 © 2008 Botanical Society of America, Inc. |
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Reproductive Biology |
Institut für Biologie—Systematische Botanik und Pflanzengeographie, Freie Universität Berlin, Altensteinstraße 6, 14195 Berlin/Germany
Received for publication 7 December 2007. Accepted for publication 9 June 2008.
ABSTRACT
Interspecific hybridization is considered a possible mechanism of plant diversification. The Andes are a hotspot of biodiversity, but hybridization in Andean taxa has so far not been investigated intensively. The current study investigates crossability in Caiophora (Loasaceae subfam. Loasoideae) by experimental interspecific hybridization of seven different species. Hand pollination was undertaken, developing fruits counted, thousand (seed) grain weights, and seed viability were examined. Cross pollination led to some fruit set in 36 of the 37 different combinations. Overall fruit set was virtually identical irrespective of the combination of parental plants. Mean germination rates were much higher in hybrid seeds, indicating a marked heterosis effect and the possible presence of an inbreeding depression in the source populations: In experimental hybridization the divergent taxa of Caiophora behave like isolated, inbred populations of a single species. Allopatry and different habitat preferences seem to be the key factors keeping the (interfertile) taxa of Caiophora apart in the apparent absence of both postmating isolating mechanisms and obvious isolating mechanisms in phenology and floral biology. Interspecific hybrids reported from the wild appear to be the result of secondary contact due to human impact.
Key Words: Andes • Caiophora • heterosis • hybridization • Peru • postmating isolating mechanisms • Loasaceae
Species limits are usually defined by some type of reproductive isolation, either premating or postmating (McDade, 1995
; Rieseberg and Carney, 1998; Rieseberg et al., 2006). Artificial hybridization experiments have thus been used in the past to infer relationships between different taxa via the degree of postmating reproductive isolation (e.g., Janczewski, 1907; Meurman, 1928; Keep, 1962; Beckmann, 1979; Wilson, 1980; McDade and Lundberg, 1982; den Nijs and Visser, 1985; Freyre et al., 2005; Mráz and Paule, 2006). It is expected that the degree of crossability between members of the same taxon is higher than crossability between different taxa (Elisens, 1989; Motley and Carr, 1998). Following a strict biological species concept, intraspecific crosses should result in full seed set with fully viable seed and viable and fertile offspring, while interspecific crosses should either not lead to seed set or to nonviable seed or the F1 generation should be sterile. In reality, some degree of crossability between taxa is often present, and the "crossability index" for fruits/seeds has been proposed as a measure for the degree of reproductive isolation (McDade and Lundberg, 1982). Elisens (1989) showed that crossability within species was close to 1, roughly 10 times as high as crossability between congeneric species and 100 times as high as between species of different genera in an extensive hybridization experiment in Scrophulariaceae (Scrophulariaceae–Anthirrhineae, Maurandyinae, involving 17 species in four genera). Crossability indices for other parameters of postmating reproductive isolation can be calculated in the same manner for data such as seed/hybrid viability or hybrid fertility (pollen viability, F1 seed set). Even if interspecific hybridization leads to seed set, the hybrid seeds should have lower germination rates and/or higher seedling mortality and/or F1 sterility compared to the parental taxa (Janczewski, 1907; Keep, 1962; den Nijs and Visser, 1985; Ramsey et al., 2003). In very general terms, the crossability index, based on any of the described parameters, should be or 1 (or close to 1) between freely interbreeding and fully interfertile populations, whereas it should be <1 between different taxa, if their taxonomic segregation is justified.
However, those hybrid plants that do develop frequently display heterosis, i.e., high survivorship and/or vigorous growth and development, irrespective and independently of their reduced fertility (Grant, 1975; Rieseberg and Carney, 1998; Ramsey et al., 2003). Heterosis and crossability are partly independent of each other: crosses between geographically closer vs. more distant populations in two forest tree species (of the genera Shorea and Syzygium, Stacy, 2001) showed that cross-fertility peaked at distances of 1–10 km between stands and was lower at higher distances (i.e., between different forest patches), but marked hybrid vigor was observed only in hybrids obtained from between-forest crosses in Shorea.
The majority of hybridization studies has been carried out in North America (e.g., Wyatt, 1990; Emms and Arnold, 1997; Campbell, 2003; Ramsey et al., 2003; Hochwender and Fritz, 2004; Burgess et al., 2005), Hawaii (e.g., Kim and Carr, 1990; Wagner et al., 1990; Whitkus, 1998; Caraway et al., 2001; Carr, 2003) and Europe (Ghazanfar, 1989; Bleeker 2003a, 2003b; Choler et al., 2004, Bleeker and Matthies, 2005; Mráz and Paule, 2006; Bleeker et al., 2007), Few experimental studies have been published from other regions such as Andean South America (Freyre et al., 2005), a particular hotspot of biodiversity. However, putative interspecific hybrids in the field have been reported from several South American plant groups (e.g., Calceolaria: Molau, 1988; Brücher, 1989; Sérsic et al., 2001; Fuchsia: Berry, 1982; Hoshino and Berry, 1989; Passiflora: Fischer, 2004).
The current study focuses on the genus Caiophora (ca. 50 spp.) of Loasaceae subfam. Loasoideae. It is the second largest genus of the subfamily (the largest is Nasa with >100 spp.) and distributed from central Argentina/Chile to southern Ecuador at altitudes ranging from 2000 to 4500 m a.s.l. Caiophora is monophyletic and has strong morphological differentiation, especially in floral morphology and function, but also in growth habit and vegetative morphology (Weigend, 1997a, b; Ackermann and Weigend, 2006). Molecular data have so far been unable to resolve the phylogeny of the genus (Weigend et al., 2004b) and the genus is therefore informally divided into several "species groups" (Weigend and Ackermann, 2003), based on a range of morphological characters (Table 1; Figs. 1, 2A, F, H, J, L, M, O; habit, petal and floral scale morphology, fruit shape). Within the species groups, the individual taxa are differentiated by minor details of flower color and morphology and leaf dissection, but are more or less homogeneous with respect to floral scale morphology, fruit morphology, and growth habit, so that species delimitation is difficult in Caiophora. Molecular data published so far indicate that sequence divergence is low in Caiophora compared to other genera of Loasaceae (trnL-trnF, psbA-trnH: Hufford et al. 2003, 2005; trnLUAA, ITS1: Weigend et al., 2004b; Weigend and Gottschling, 2006), and the numerous taxa may go back to a relatively recent radiation. Many of the currently recognized species are widely polymorphic and fall into numerous local races, differing in characters such as floral color and morphology, fruit size, leaf morphology, and growth habit (Weigend, 1997b; Weigend and Ackermann, 2003; Ackermann and Weigend, 2007). Flower ecology of Loasaceae subfam. Loasoideae has been studied intensively (Harter, 1995; Schlindwein, 1995, 2000; Wittmann and Schlindwein, 1995; Schlindwein and Wittmann, 1997; Ackermann and Weigend, 2006; Weigend and Gottschling, 2006), revealing a range of floral types and pollination syndromes. However, in Caiophora only a relatively small range of syndromes has been reported, with mixed pollination by hummingbirds and long-tongued bees in the majority of taxa (Ackermann and Weigend, 2006).
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was the first to report hybridization in Caiophora and named a total of three putative hybrids from northern Argentina. Brücher (1986, 1989) also reported interspecific hybrids between various winding species of Caiophora in northwestern Argentina and southern Bolivia, especially between C. lateritia (Hook.) Klotzsch, C. aconquijae Sleumer, and C. hibiscifolia (Griseb.) Urb. & Gilg. More recently, the type collection of Caiophora pauciseta Killip [= C. peduncularis (C.Presl) Weigend and Mark.Ackermann] was recognized as coming from a hybrid population between C. peduncularis (C.Presl) Weigend and Mark.Ackermann and C. carduifolia C.Presl, including both parental species plus intermediate specimens (Weigend and Ackermann, 2003). In the past 15 years, we carried out a total of 65 wk of field studies in Andean South America, leading to >200 collections of Caiophora. These include several collections that we assume to represent interspecific hybrids (Table 3, Fig. 2G, I, K, N), since they are morphologically intermediate between their putative parental taxa, both of which are present in the collection area in all cases (Fig. 2F, H–J, L, M, O). All putative interspecific hybrids in Caiophora appeared to have normally developed capsules and seeds. In the literature data and our own observations, 11 apparently fertile interspecific hybrids are thus reported for Caiophora, all of them hybrids between widely divergent species (mostly belonging to different species groups as defined in Weigend and Ackermann, 2003). However, as Rieseberg and Wood (2006, p. 6) pointed out, "The lack of association between contemporary hybridization and taxonomic difficulties may be an artifact of the difficulty of recognizing hybrids where taxa are not distinct to begin with." This may hold true for Caiophora, for which hybrids between the various "species" or local races of the C. cirsiifolia, C. carduifolia, or C. chuquitensis groups would be difficult to identify in the field and next to impossible to recognize in the herbarium.
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MATERIALS AND METHODS
Sampling
Putative interspecific hybrids are known from most groups of Caiophora. Our own observations include putative hybrids between the C. chuquitensis and the C. cirsiifolia or C. carduifolia species groups (Table 3) and a hybrid between the C. cirsiifolia and C. carduifolia species groups (Weigend and Ackermann, 2003). We therefore included representatives of these three species groups in our experiment. Additionally, two representatives of the C. lateritia species group and one of the C. coronata group were included because putative hybrids between species of these groups have been reported (Sleumer, 1955; Brücher, 1986, 1989). Three different geographical races of C. cirsiifolia (Fig. 1I–K) were also included in the experiment. This sampling should enable us to compare the crossability between more distantly to more closely allied taxa.
Experimental crosses
Voucher data for all accessions used in this study are summarized in Appendix 1. Abbreviations for the departments were added to the name throughout text, figures, and tables to indicate the source location of each accession. Seeds were collected in the wild, each seed lot was mixed from several seed capsules from different plants for each accession, and thus each accession represents a population subsample. We will refer to "accessions" for these subsamples and infer conclusions about the populations in the discussion based on these population subsamples. All plants were cultivated in the greenhouse in Berlin in the same compartment and thus under identical conditions (lighting, temperature, soil, pot size). The same individual plants were used for both inter- and intraspecific crosses. Artificial interspecific and intraspecific cross-pollinations were done in April–May 2004. Reciprocal cross-pollinations were carried out between seven species of Caiophora (one represented by three different morphotypes), representing five different species groups sensu Weigend and Ackermann (2003). All species of Caiophora are proterandrous, but of all the Caiophora species so far cultivated (ca. 25 species and multiple different morphotypes) require hand-pollination in the absence of pollinators: fruit set was not observed in any of the several hundred flowers that were not hand-pollinated. Only one species so far cultivated [C. contorta (Desr.) C.Presl] is self-pollinating. Caiophora contorta was not used for crosses, i.e., none of the Caiophora taxa used in the experiment is self-pollinating. Flowers used as pollen recipients were nevertheless emasculated before anther dehiscence (Fig. 2B) to avoid accidental self-pollination during manipulation. Also, greenhouse windows were closed, precluding pollinator activity during the experiments. A total of 230 flowers were hand-pollinated (Table 4): In six species (including C. cirsiifolia with three morphotypes), 20 flowers each were used (five flowers each for pollination with pollen from three other species and five for intraspecific pollination, 120 flowers total). In the other two species, 45 flowers each were used (five flowers each for hybridization with eight other species and five for intraspecific pollination, 90 flowers total). When flowers reached the carpellate phase (fully developed stigma, Fig. 2C), they were dusted twice with dehisced anthers of the pollen donor on consecutive days. Each flower was then marked with a color-coded wire. Capsules matured after four to six weeks (Fig. 2E). Maturity is recognizable by the color change (green to yellow/brown) and the opening of longitudinal sutures. Fully developed capsules were counted and collected in paper bags. With the start of summer, especially with high temperatures and the onset of acariasis, some of the taxa [C. carduifolia (AP) and C. cf. madrequisa, to some degree C. canarinoides] began to die, producing few or no mature capsules (Fig. 2D), which led to the loss of some fruits (from both interspecific and intraspecific pollination).
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% fruit set F1) / ((% fruit set P1 + % fruit set P2)/2).
Seed masses
Mature seeds from capsules resulting from cross pollination and the seeds of the parental species were investigated for seed mass. One hundred seeds were counted out and weighed with a Sartorius R2000D laboratory balance and calculated as thousand grain weight (tgw). Means and standard deviation (SD) are given for ease of comparison.
Seed germination
One hundred seeds from each crossing experiment were germinated by placing them onto moist filter paper in sealed plastic petri-dishes (Whatmann’s No.1 filter paper moistened with water, kept in daylight at ca. 18–21°C). Germination was measured by counting and removing the germinated seeds in the course of the subsequent three weeks, after which no further germination was observed. Germination rates were tabulated and crossability indices calculated from them. Crossability indices for seed viability were obtained for the three types of cross pollination specified (see fruit set) and calculated by dividing the germination rate obtained from crosses between species/accessions (germ.F1) by the mean germination rate of seeds obtained from the corresponding cross-pollination between individuals from the same accession ((germ.P1 + germ.P2)/2). The following formula was used to obtain crossability indices for germination data: CI = (germ.F1) / ((germ.P1 + germ.P2)/2).
RESULTS
Fruit set
Experimental crosses between both closely allied and widely divergent species of Caiophora (parental species: Figs. 1, 2A, 2F) were equally successful (Table 4). A total of 37 crosses between different geographical races or species were attempted, usually with each individual accession serving once as pollen donor and once as pollen recipient for any given combination. Thirty-six of the crosses resulted in fully developed capsules; only one interspecific combination did not lead to fruit set (C. deserticola x C. pentlandii). Fruit set from cross pollination between species from different species groups (74%) and between individuals of the same accession (75%) was virtually identical (CI: 1). The (fewer) cross pollinations between closely allied taxa led to marginally higher fruit set (83%, CI: 1.1).
Seed masses
Seed masses from inter- and intraspecific pollination in Caiophora are summarized in Table 5. They show only minor differences. Mean values for seed masses of the parental species obtained from cultivation and collected in the wild are close to the mean values for hybrids with the same maternal accession. Standard deviations (of tgw) for hybrids with the same maternal accession range between 4.1 and 28.3%, means of the maternal accession are usually within the range of this hybrid SD. Seed mass variation of a factor two (in viable seeds) is common within individual species/populations of Loasoideae (Weigend et al., 2004a), so that all seeds obtained appeared to be normally developed.
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germ.F1/ ((germ.P1 + germ.P2)/2)] obtained from the germination rates of hybrid seeds range from 0 to 21.5. Seeds resulting from cross-pollination between different species/accessions generally had higher germination rates than those from intraspecific cross-pollination. Overall germination rate was 56% in seeds from cross pollination between species from different species groups and 46% in seed obtained from crosses between geographical races/closely allied species. Conversely, average germination is only 19% in seeds obtained from cross pollination within the same accession. Overall crossability indices calculated on the basis of seed germination are thus 3.02 for crosses between species from different groups and 2.49 for crosses between geographical races/closely allied species. Crossability indices were higher than 1 in 25 sets of hybrid seeds (two-thirds of the sample), i.e., viability was higher in seeds obtained from hybridization than in seeds from same-accession pollination. Only 11 interspecific combinations (one-third of the sample) yielded seed that was less viable or equally viable as seed from same-accession pollination (CI 
1). Some of the highest germination rates were obtained with hybrid seeds from crosses between remotely related species (compare Table 1, C. deserticola x C. canarinoides: 96%, C. deserticola x C. carduifolia: 95%). Conversely, same-accession cross pollination yielded seeds with low germination rates in some cases (e.g., C. pentlandii: 4%, C. cirsiifolia (CA1): 0%, C. chuquitensis: 0%, C. madrequisa: 2%).
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Possibility of interspecific hybridization
Caiophora can be freely hybridized across species and species groups. Successful hybridization between divergent lineages (such as the C. cirsiifolia and the C. chuquitensis group) inferred from field observations (Tables 2, 3) is confirmed as possible by the experimental data. Fruit set obtained in inter- and intraspecific crosses is nearly identical, and postmating isolating mechanisms are apparently absent in Caiophora. The high crossability of Caiophora is in line with the conclusion of Ellstrand et al. (1996), that natural hybridization is more prevalent in outcrossing perennials. However, at present there is no evidence for the presence of reproductive modes stabilizing hybridity "such as agamospermy, vegetative spread, or permanent odd polyploidy" (Ellstrand et al., 1996, p 5090.). Germination rates of hybrid seeds on average far exceed the germination rates of seed from within-accession cross-pollination, which can be seen as a case of hybrid vigor (Grant, 1975). The crossability indices calculated from seed germination further indicate that hybrids between highly divergent parental species have germination rates that are identical to or higher than those between closely allied taxa. Viability, vigor, and/or fertility of the F1 plants are usually reduced in interspecific hybrids between distantly related taxa (Sawant, 1958; Keep, 1962; Goldschmidt, 1964; den Nijs and Visser, 1985; Rieseberg and Carney, 1998; Burke and Arnold, 2001; Sérsic et al., 2001), whereas heterosis (hybrid vigor) is expected in crosses between geographical races of individual species (Grant, 1975). A high crossability index (
1) and a marked heterosis effect are expected in crosses between isolated, inbreeding populations of individual taxa (Fenster and Galloway, 2000; Sheridan and Karowe, 2000; Weller et al., 2005; Busch, 2006; Heliyanto et al., 2006). Thus, in our hybridization experiment, all taxa and accessions of Caiophora behaved like isolated, inbred populations of a single species, with overall crossability indices based on seed germination >>1. This is particularly striking because in other studies crossability decreased with increasing geographical distance between populations of the same species within a relatively narrow geographical range (Wyatt, 1990; Stacy, 2001) or allopatric populations of the same morphospecies had high degrees of reproductive isolation (Grundt et al., 2006). Germination rates are partly dependent on the choice of the pollen donor/pollen recipient, and some (weak) asymmetrical crossing barriers are apparently in place (compare Tiffin et al., 2001): The figures show striking differences in the CIs of individual taxon combinations, depending on the choice of the male and female parent. Thus, the germination rates of seeds obtained from C. deserticola x C. madrequisa have a CI of 3.9 with C. deserticola as female parent, but a CI of 0 with C. madrequisa as female parent; similar trends can be observed in other species combinations (Table 7).
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indicate that the pollination biology of the species groups here investigated is little differentiated; most taxa fell into a group pollinated by long-tongued bees and/or hummingbirds, and pollinator specificity is likely low. Accidental interspecific cross pollination is likely to occur where more than one species is found in a single area. There is direct observational evidence for two species sharing the same pollinator in the case of C. deserticola and C. cirsiifolia in Moquegua, where both species are visited and apparently pollinated by the same species of Centris (long-tongued bees, Apidae; Ackermann and Weigend, 2006). Incidentally, an interspecific hybrid has been documented between these two species in the same region (Table 3). Neither does phenology provide an isolating mechanism in Caiophora because all species have their peak flowering time at the end of the rainy season in the Andes (ca. March–May in Peru). Ecogeographic isolation remains the only obvious premating isolation mechanism in Caiophora; there is usually geographical and/or altitudinal segregation between different species of Caiophora, both between and within species groups. Altitudinal distributions of species usually overlap slightly across their geographical range (compare Tables 1, 3), but in any given region different species are not usually found at the same elevation. In many cases there is additional ecological differentiation, with, e.g., the erect (suffruticose) species of the C. chuquitensis group found in shallow, often open soils and the winding species of other groups largely restricted to scrub and scrub forest. Table 3 gives habitats and the elevational ranges of the parental taxa and the habitat and elevation at which the putative hybrids were collected. In three of the four cases, the hybrids were found far above the mean altitudinal range of one of the parental species and in the range of the second parental species. In these three cases, hybrids were found near roads coming from lower elevations with natural stands of the other ("azonal") parent, so that both disturbance and seed transport by man may have played a role in hybrid formation. The fourth case of hybridization reported apparently also goes back to human impact. Both C. deserticola and C. cirsiifolia are abundant in Depto. Moquegua at the same elevations, but whereas C. deserticola is a shrubby species restricted to rock faces and dry scree slopes, C. cirsiifolia is a winding species restricted to moister parts of the scrub-forest, usually in gullies and near seepage areas, so that isolation is maintained under natural conditions. The hybrid was collected in a place where agricultural terraces had been built right into a dry scree slopes with natural stands of C. deserticola. The terraces were fenced with hedges and irrigated and provided an excellent manmade habitat for C. cirsiifolia, so that the two species grew less than 5 m apart.
Conclusion
Hybrids in Caiophora are readily produced even between morphologically divergent species groups, differing in floral and growth morphology, distribution, and ecology. Postmating isolating mechanisms are apparently absent. Taxa are primarily kept apart by ecogeographical isolation. Secondary contact from human impact leads to hybrid formation, while under natural conditions the efficiently wind-dispersed seed of Caiophora (Weigend et al., 2004a, 2005) may ensure the occasional contact between different taxa. Problems with taxon delimitation in Caiophora are likely at least partly due to the presence of specimens with "mixed" or "intermediate" morphological characters as a result of hybridization and possibly introgression. The low sequence divergence observed in Caiophora (Hufford et al., 2003, 2005; Weigend et al., 2004b) correctly reflects a close relationship and possibly recent radiation of Caiophora in the Andes. However, the morphological and ecological differences between taxa clearly argue that they largely behave as distinct lineages under natural conditions and should be kept taxonomically separate. Many natural populations of Caiophora are short-lived and isolated and often have few individuals, which may explain the relatively low seed viability of same-population cross-pollinated seeds, indicating that at least some natural populations of Caiophora are subject to inbreeding depression. The high degree of interspecific crossability of Caiophora is possibly best compared to similar observation made on recently diverged species of island floras (Wagner et al., 1990; Motley and Carr, 1998). Hughes and Eastwood (2006, p. 10334) demonstrated an extraordinary rate of speciation resulting in a large number of geographically isolated, but closely related species of the genus Lupinus in the high Andes and called this phenomenon an "island radiation on a continental scale." A similarly rapid allopatric "island radiation" may have taken place in Andean Caiophora, also leading to morphologically highly distinct, but young and, in this case, (still?) interfertile lineages. Further studies on the F2 and F3 generations are now under way to investigate the occurrence of a possible hybrid breakdown and the stability of novel characters or character combinations in subsequent generations to understand the possible role of hybridization in the evolution of the genus.
Appendix 1. Vouchers for accessions used for experimental crosses and for putative hybrids and corresponding parental taxa observed in the field (+ C = herbarium sheets from cultivated plants deposited in BSB; abbreviation after plant names author indicate department of origin in Peru).
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FOOTNOTES
1 The authors express their gratitude to L. Rieseberg (Vancouver) and S. Renner (Munich) for helpful comments on the manuscript. The authors thank A. Cano and M. I. La Torre (Lima, Peru), F. Luebert (Santiago, Chile), E. Rodríguez (Trujillo, Peru), N. Salinas (Cuzco, Peru), H. Förther (München, Germany), N. Dostert, T. Henning, D. Kollehn, O. Mohr, C. Schwarzer and K. Weigend (Berlin, Germany) for help in the field and collecting; Prof. Dr. H. H. Hilger for space and funds for this study. Funds kindly provided by the following institutions are gratefully acknowledged: Studienstiftung des Deutschen Volkes, Deutscher Akademischer Austauschdienst, Lewis B. and Dorothy Cullman Laboratory for Molecular Systematics Studies at the New York Botanical Garden, Deutsche Forschungsgemeinschaft (Grant-nr.WE 2330/1), botconsult GmbH. 
2 Author for correspondence (e-mail: ackermal{at}zedat.fu-berlin.de)
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