Proc. Nati. Acad. Sci. USA Vol. 91, pp. 3-10, January 1994 Review Modes and origins of mechanical and ethological isolation in angiosperms Verne Grant Department of Botany, University of Texas, Austin, TX 78713 ABSTRACT Mechanical and etholog- 1937-1950. Building on these early The breakdown of the diverse phenom- ical isolation between species is wide- works, I showed that the preconditions ena of floral isolation into different forms spread in angiosperms with specialized for reproductive isolation at the stage of is helpful in relation to a discussion of the animal-pollinated flowers, being recorded pollination are widespread in an- origin of floral isolation. We find, as in 29 species groups belonging to 27 genera giosperms with complex floral mecha- might be expected, that no one mode of and 16 families. Mechanical isolation oc- nisms (4). evolution will account for every form of curs in two forms. (i) The common type, My early paper (4) recognized etho- floral isolation in every plant group. Thus designated the Salvia type, operates when logical as well as mechanical isolation in this paper will examine the diverse ori- two or more species of flowers are adapted angiosperms. Mechanical isolation can gins of floral isolation. for different groups of pollinators with occur when two or more plant species different body sizes and shapes. (it) In the have different flower structures that re- Broad Evidence for Floral Isolation / Pedicularis type two flower species have duce or prevent interspecific pollina- the same species of pollinator but pick up tion. Ethological isolation takes place Examples of floral isolation in nAture pollen from different parts of the pollina- when specialized flower-visiting ani- have now been reported in many plant tor's body. Four forms of ethological iso- mals make preferential visitations to one groups in many geographical areas. The lation are recognized. ('l In the Aqulegia species of flower which they recognize cases known to me are listed in Table 1. type, which is widespread, ethological iso- by its specific shape, color, markings, These cases occur in 29 species groups in lation is a side effect of mechanical isola- and/or scent. Mechanical and etholog- 16 families. They leave little doubt that tion. (u) The flower-constancy type, as the ical isolation are likely to be combined floral isolation is a real barrier to gene name suggests, is based on flower-constant in actual cases, making it useful to group exchange between species in many ani- foraging behavior. (ii) In the Ophrys type, them in a mal-pollinated plant groups. floral scents attract male bees or wasps collective mode, floral isola- Floral isolation depends on floral spe- and play a role in their mating behavior; tion. cializations. It will be noted that all but a different species of flowers, often orchids, After 1950 opinion regarding floral few of the cases in Table 1 occur, as have different scents and attract different isolation was divided between support would be expected, in genera and fami- sets of hymenopteran species. (iv) The (5) and skepticism (6). It was obviously lies with complex floral mechanisms. The monotropy type occurs in plants pollinated necessary to document floral isolation Scrophulariaceae and Orchidaceae to- by hymenopterans with species-specific or between sympatric species in nature. gether account for 10 of the 29 known group-specific flower preferences for nu- This was done by my students and my- examples. tritive purposes (monotropic and oligotro- self in the next few years (1952-1964) in One family with complex flowers that pic bees and fig wasps). Three modes of Aquilegia (7), Penstemon (8), Pedicu- is missing from Table 1 is the Asclepi- origin of floral isolation are confirmed by laris (9), and Salvia (10). In these cases adaceae. Years ago it was cited as a evidence: (') mechanical and ethological the floral isolation is primarily mechan- group in which mechanical isolation was isolation arising as a by-product of abo- ical but is supplemented by ethological well developed (3, 4, 47). But later stu- patric speciation, (fi) ethological isolation isolation. dents have downgraded mechanical iso- developing by selection for reproductive Since that period a much larger body of lation in the genus Asclepias to a pro- isolation per se, and (Wi) mechanical isola- evidence has been obtained from more cess of secondary or negligible impor- tion arising as a by-product of character plant groups. One of the purposes of this tance (48, 49). This is a group in which displacement. Mode of origin i accounts paper is to present the broader data base the early predictions were plausible but for the Salvia and Aquilegia types of iso- that now exists. The broader data base have not stood up under closer inspec- lation in nine known species groups and makes it possible to recognize different tion. Since an expectation of mechanical for the Ophrys type in one group. Mode of modes of mechanical and ethological iso- isolation in the Asclepiadaceae is still origin u accounts for the flower-constancy lation. A second purpose of this review is warranted, further search for valid ex- type of ethological isolation in two species to outline these modes. amples is desirable. groups. Mode of origin ui explains me- A question which remains problemat- Mechanical isolation is the main mode chanical isolation in two groups. Sympat- ical is the origin of floral isolation. This in many of the examples in Table 1. ric origin of floral isolation by hybrid subject was discussed in a preliminary Ethological isolation is often complemen- speciation and by flower constancy has way in my early paper (4), where both tary to mechanical isolation (e.g., in Aq- been proposed, but these modes are un- allopatric and sympatric models were uilegia, Polygala, Penstemon, Pedicu- documented and improbable. considered, but the models were theo- laris), confirming the usefulness of the retical. What is needed is a modern collective mode, floral isolation. Etho- The possibility that differences between analysis of the problem on the basis of logical isolation plays a primary role in related plant species in flower structure our present expanded data base and in several groups (Hedysarum, Cercidium, may function as a mechanical isolating the light of our current understanding of Phlox, Ophrys). mechanism was suggested by Dobzhan- speciation. Such an analysis is pre- The strength of the floral isolation sky (1, 2) and Stebbins (3) in the period sented here. varies over a wide range. It is very 3 4 Review: Grant Proc. Natl. Acad. Sci. USA 91 (1994) Table 1. Groups of related species which are mechanically (M) and/or ethologically (E) isolated in nature, listed by family Mode of Species group Area Pollinators isolation Refs. Ranunculaceae Aquilegia formosa subgroup and A. caerulea W. North America Hummingbirds (A. f.), M, E 7,11,12 subgroup hawkmoths (A. c.) Berberidaceae Epimedium grandiflorum, E. sempervirens, and E. Japan Bees E 13 trifoliatobinatum Papaveraceae Papaver rhoeas, P. dubium, and three other species Great Britain Bumblebees, honeybees E 14 (inferred) Leguminosae Cassia leiophylla and C. bicapsularis Mexico Bumblebees and other large M 15 bees (C. b.), smaller Ptiloglossa bees (C. 1.) Cercidium floridum and C. microphyllum California Bees E 16 Hedysarum boreale and H. alpinum Alaska Bumblebees, Megachile bees E 17 Polygalaceae Polygala vauthieri and P. monticola Brazil Bees M 18 Onagraceae Fuchsia encliandra and F. parviflora Mexico Hummingbirds (F. e.), M, E 19 bumblebees (F. p.), where sympatric Euphorbiaceae Dalechampia brownsbergensis and D. fragrans Surinam Male euglossine bees E 20 Balsaminaceae Impatiens capensis and I. pallida E. North America Hummingbirds (I. c.), M 21 bumblebees (I. p.) Polemoniaceae Phlox pilosa and P. glaberrima Illinois and Indiana Butterflies E 22, 23 Phlox drummondii and P. glaberrima Illinois (synthetic Butterflies E 23-25 population) Ipomopsis aggregata and I. tenuituba W. North America Hummingbirds (I. a.), M, E 12, 26 hawkmoths (I. t.) Solanaceae Solanum grayi and S. lumholtzianum Mexico Large bees (S. l.), small bees M 27 (S. g.), where sympatric Scrophulariaceae Mimulus cardinalis and M. lewisii W. North America Hummingbirds (M. c.), M 28 bumblebees (M. l.) Diplacus puniceus, D. longiflorus, and D. calycinus California Hummingbirds (D. p., D. l.), M 29, 30 hawkmoths (D. c.) (inferred) Penstemon centranthifolius, P. grinnellii, and P. California Hummingbirds (P. c.), carpenter M, E 8 spectabilis bees (P. g.), wasps (P. s.) Pedicularis groenlandica and P. attollens California Bumblebees M, E 9, 31, 32 Rhinanthus minor and R. serotinus Europe Bumblebees M, E 33 Labiatae Salvia apiana and S. mellifera California Carpenter bees (S. a.), M, E 10 medium-sized and small bees (S. m.) Monarda didyma and M. clinopodia E. North America Hummingbirds (M. d.), M, E 34 bumblebees (M. c.) Campanulaceae Lobelia cardinalis and L. siphilitica E. North America Hummingbirds (L. c.), M, E 35, 36 bumblebees (L. s.) Haemodoraceae Anigozanthos manglesii and A. humilis Australia Wattle birds (Meliphagidae) M, E 37 Musaceae Heliconia umbrophila, H. irrasa, and other species Costa Rica Hermit and nonhermit M 38, 39 hummingbirds Orchidaceae Ophrys insectivora, 0. speculum, and other species Europe and North Africa Male bees and wasps M, E 40, 41 Ophrys fusca and 0. lutea Algeria Male Andrena bees M, E 42 (inferred) Platanthera bifolia and P. chlorantha Europe Moths M, E 43 Stanhopea tricornis and S. bucephalus Ecuador Eulaema bees M, E 44, 45 Angraecum compactum and Neobathiea Madagascar Hawkmoths M, E 46 grandidierana (closely related though placed in different genera) Review: Grant Proc. Natl. Acad. Sci. USA 91 (1994) strong in Ophrys (41), Mimulus (28), and blebee flowers and are pollinated by the ported in the early years in Antirrhinum Pedicularis (9, 31, 32). In Aquilegia and same species of Bombus (B. bifarius and (55), Gilia (4), Clarkia (56), Papaver Ipomopsis, on the other hand, the floral B.