Is Psammophily an Evolutionary Dead End? A Phylogenetic Test in the Genus Willemia (Collembola:...

Cladistics 16, 255–273 (2000)

doi:10.1006/clad.2000.0131, available online at http://www.idealibrary.com on

Is Psammophily an Evolutionary Dead End?A Phylogenetic Test in the Genus Willemia(Collembola: Hypogastruridae)

Cyrille D’HaeseUPRES-A 8043 CNRS, Laboratoire d’Entomologie, Muse

´um national d’Histoire naturelle, 45, rue Buffon,

F-75005 Paris, France

Accepted December 7, 1999

The law of the unspecialized states that specialized taxahave evolved from more generalized ancestors. Moreover,it is usually assumed that ecological specialization isirreversible and hence leads to extinction. This studyaims to test these assumptions using a phylogeneticframework in a case study within the springtail genusWillemia and its diverse life habits. This genus is repre-sented mostly by loam-dwelling species (generalized con-dition), but some species are psammophilous, living insandy habitats (specialized condition). Fifty-two mor-phological characters were examined in 34 of the 36species of the genus and in three outgroups. The cladisticanalysis yielded two most parsimonious trees (treelength 124 steps; consistency index 0.56; retention index0.86). The evolution of psammophily versus loam-con-fined life is compared to the cladogram: unexpectedly,psammophily is not an evolutionary innovation thatoccurred once in a monophyletic group; the evolutionaryscenario that parsimoniously fits the phylogeny suggeststhat psammophily is ancestral to the genus Willemia and
reversed twice to loam-confined life. These results dem-onstrate that habitat generalists can evolve from habitatspecialists and therefore that habitat specializations arenot necessarily an evolutionary dead end. Many other
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seemingly specialized characters may be shown to beequally malleable. q 2000 The Willi Hennig Society

INTRODUCTION

In addition to the well-known rule of Cope (evolu-tionary trend toward increasing body size within alineage), Cope stated “the law of the unspecialized,”which considers that ancestors of successful groupstended to be unspecialized, i.e., not restricted to defi-nite habitats, climate, or food (Cope, 1896). Amongothers, Simpson (1944), Mayr (1942, 1988), and Sugi-hara (1980) developed the same ideas, and these state-ments are now widely accepted: “In virtually everytaxon, species with morphological and physiologicaladaptations to specialized habitats, resources, andways of life have evolved from more generalized ances-tors” (Futuyma, 1998: 698; see also Futuyma and Mor-
eno, 1988).
Cope (1896: 173) added that “the specialized typesof all periods have been generally incapable of adapta-tion to the changed conditions”; in other words, he

256

considered that specialization leads to extinction. Simi-larly Mayr (1942: 294) considered that “every phyloge-netic sequence leads from generalized primitive formsthrough more and more specialized forms, until it fi-nally ends in overspecialization and extinction.” Infact, specialization is often thought to lead to an evolu-tionary dead end and ultimately to extinction (Dollo,1903; Futuyma and Moreno, 1988; Huxley, 1942;Rensch, 1959; Simpson, 1953). Compared to specialists,generalists often have a wider range of features thatallow them to develop new variations to fit to environ-mental modifications. These ideas referred to the sup-posed inability of a taxon to reacquire an ancestral state(unidirectional evolutionary trend); in other wordsthey referred to the concept of evolutionary irrevers-ibility known as Dollo’s law (Dollo, 1893, 1922; seeGould, 1970, for a review). Hitherto, irreversibility isan almost unchallenged rule (e.g., Bull and Charnov,1985; Laurent, 1983; Simpson, 1953; Wagner, 1982),even if some exceptions were recorded on a small scale(Laurent, 1964; Lande, 1978; Macbeth, 1980).

To determine character polarity and test the orderof appearance of life history traits, a phylogeneticframework is needed. This applies also to the macro-evolutionary patterns involving the evolution of gener-alists versus specialists. The purpose of this study is toprovide a phylogenetic test of Cope’s two evolutionaryhypotheses, namely, specialized species evolved fromgeneralized ancestors and specialization ends in extinc-tion, in the springtail genus Willemia.

The genus Willemia Borner, 1901 (Collembola, Hypo-gastruridae) is represented mostly by loam-dwellingspecies living in weak acidic soils (Hagvar, 1983; Ponge,1980, 1993; Ponge and Prat, 1982; Arbea and Jordana,1986), but some species are psammophilous (sand-dwelling animals), living in terrestrial sandy soils (Ster-zynska and Ehrnsberger, 1997; Thibaud and Massoud,1988; Thibaud and Lee, 1994; Thibaud and Christian,1989; Thibaud and Weiner, 1997).

According to Lincoln et al. specialization is an “evolu-tionary adaptation to a particular mode of life or habi-tat” (1998: 280). Thriving in interstitial sandy habitats(psammophily) is considered as a highly specializedecology (e.g., Coineau and Massoud, 1977) comparedto living in loamy soils, a trait that is widespread in
Collembola, since it requires both morphological andphysiological specializations (Thibaud and Christian,
Copyright q 2000 by The Willi Hennig SocietyAll rights of reproduction in any form reserved

Cyrille D’Haese

1997). Three main factors explain why ecological spe-cializations are needed in sandy soils: (1) hygrometry:in Collembola, the highest population densities andspecies richness are found in humid environments(Choudhuri and Roy, 1967; Hazra and Choudhuri,1983; Poole, 1961; Rusek, 1989), whereas Collembolain sandy soils must cope with water deficiency (Thi-baud and Christian, 1997; Vannier, 1983); (2) smallamount of organic matter available in sandy habitats(oligotrophy): species numbers increase with increas-ing soil fertility (Choudhuri and Roy, 1967; Hagvar,1983; Hazra, 1978); it has been clearly shown that themain distributional pattern of Collembola could bebroadly related to the level of soil fertility (Hagvar,1982, 1983, 1984); (3) Granulometry size: the collembo-lan fauna is not directly influenced by the vegetationtypes but is related to soil type or soil structure(Hagvar, 1982; Ponge, 1993; Roske, 1989). Sandy habi-tats have a granulometry size less than 1 mm andsand is a cohesionless sediment; as such, it is the lessfavorable environment for arthropods in general andCollembola in particular (Vannier, 1975). As a conse-quence of these constraints, few species with low popu-lation densities are found in sandy habitats (Petersen,1965; Poinsot, 1966; Christian and Thibaud, 1988; Thi-baud and Christian, 1989). Within the springtails, thefamily Hypogastruridae comprises 40 genera, of whichonly 6 have more than 20 species, including Willemiawith 36 species. Furthermore this genus has a world-wide distribution; hence it can be considered as a suc-cessful taxon from an evolutionary point of view.

Since both life habits are found in Willemia (the spe-cialized one: psammophily, and the generalized one:loam-confined life), this genus is appropriate for test-ing the law of the unspecialized. In that way the evolu-tion of ecological adaptation to soil can be studiedin the genus in terms of psammophily versus loam-confined life. The law applied to the genus Willemiawould predict that psammophily is a uniquely derivedcondition; actually, the common supposition states thatspecialization is irreversible and hence a derived condi-tion (Futuyma and Moreno, 1988). Is psammophily aderived evolutionary event that occurred once in a
monophyletic group as Cope’s law and commonsense indicate?

Is Psammophily an Evolutionary Dead End?

MATERIALS AND METHODS

The study deals with 34 of the 36 species known inWillemia (Appendix 1). The remaining species (W. bisetaChristiansen and Bellinger, 1980 and W. bulbosa Bonet,1945) were excluded because they could not be studiedin detail (short descriptions in the original papers andno material available for study). Three groups are rec-ognized in the genus Willemia (Potapov, 1994): (1) theanophthalma group (D’Haese, 1998) with 8 species; (2)the denisi group (Potapov, 1994) with 8 species; and(3) the buddenbrocki group (D’Haese and Weiner, 1998)with 10 species (see Appendix 1). The phylogeneticanalysis allows one to establish whether these groupsare monophyletic or not. For the last group, a cladisticanalysis of 26 characters in 14 species (including the10 species of the buddenbrocki group) already arguedfor its monophyly (D’Haese and Weiner, 1998); thusthe present analysis with more characters and morespecies is a test of the robustness of that previous phy-logenetic hypothesis. An identification key of the spe-cies of the genus Willemia is given in Appendix 2.

Fifty-two characters were used for the phylogeneticestimate. Chaetotaxy is one of the few morphologicalstructures that provide characters for species recogni-tion and phylogenetic reconstruction in Collembola.The shape and number of the blunt antennal sensillaalso provide characters. The number of postantennalorgan vesicles, anal spines, and shape of setae s arealso included in the matrix. On the head, the setaenomenclature is taken from Cassagnau (1974). On tho-racic and abdominal terga setae, nomenclature followsthe three-row system (a, m, and p) (Figs. 1A and 1B),developed by Yosii (1956, 1971) and Grow and Chris-tiansen (1974). On antennal segment IV, sensilla no-menclature follows Arbea and Jordana (1986) and Pota-pov (1994) with external sensilla e1, e2, and e3, dorsalsensillum d, and internal sensilla i1 and i2 (Figs. 2Ato 2D).

Question marks represent either inapplicable or un-known characters. Autapomorphies were excluded, sothat only potentially informative characters are kept.All character states are polarized through outgroupcomparison with three species belonging to the Hypo-gastruridae genera Hypogastrura, Orogastrura, and Xen-
yllogastrura (Appendix 1). Each one is taken as an out-group (three analyses were performed), so that the

257

monophyly of Willemia can be tested (Barriel and Tassy,1998). Xenyllogastrura was included as an outgroupbecause Gisin (1960) regarded it as a subgenus of Wil-lemia. The data matrix (Table 1) was analyzed withHennig86 (Farris, 1988) applying the ie* option, usingnonadditive coding for characters (unordered charac-ters). The consistency index (Kluge and Farris, 1969)and retention index (Farris, 1989) were given. Bremer(1988) support indices were calculated using PAUP3.1.1 (Swofford, 1993). Character distributions were ex-amined with the program CLADOS 1.2 (Nixon, 1992).

The phylogenetic framework leads us to test macro-evolutionary features according to Brooks and McLen-nan: “only trees produced in accordance with phyloge-netic systematic principles provide the robust estimatesof genealogical relationships that are necessary precur-sors for historical ecological studies” (1991: 62). Thismethodology using phylogenetic tests of evolutionaryscenarios was widely developed; see, e.g., Coddington(1988), Carpenter (1989), Grandcolas et al. (1994), Millerand Wenzel (1995), Desutter-Grandcolas (1997), Packer(1997), Wenzel (1997), and Grandcolas (1997) for recentdevelopments. Psammophily versus loam-confinedlife is analyzed using phylogenetic analysis to optimizethese macroevolutionary features onto the cladogramof the genus Willemia.

Ecological habitats are considered as attributes(Mickevich and Weller, 1990; Deleporte, 1993). Theyare coded under four states: species found in guano(G), species found in sand only (strictly psammophi-lous) (P), species found in both sandy and loamy habi-tats (P/L), and species found in loamy habitats only(L) (Table 3). Since adaptation to sandy habitats is ahighly specialized ecology, even a species living occa-sionally in sandy habitats is specialized. Consequently,in a second analysis, strictly psammophilous speciesand species found in both sandy and loamy habitatsare coded under the same attribute: psammophilysensu lato versus strictly loam-dwelling species. All traitstates are treated unordered and parsimoniously opti-mized on the phylogenetic tree. The most-parsimoni-ous scenario that fits the phylogenetic pattern is takenas the best estimate of the evolution of the attribute.

The ecology of the species is easily determined be-cause of the methods used for sampling Collembolain soil biology studies. Usually, soil samples are
brought into the laboratory and specimens are ex-tracted with a Tullgren funnel or by flotation method

2 lle D’Haese

CA

58 Cyri

FIG. 1. Dorsal chaetotaxy (scale bars, 0.1 mm). (A) Willemia similis; (B) W. annapurna.

opyright q 2000 by The Willi Hennig Societyll rights of reproduction in any form reserved

wandae 10030 03111 11311 11121 00133 11100 01101 11111 11111 11111 01

t.
Note. Character numbers correspond to the character list in the tex
(particularly for sandy habitats) (Andre and Noti,

Is Psammophily an Evolutionary Dead End? 259

TABLE 1

Data Matrix of 52 Characters in 3 Outgroups and 34 Species of the Genus Willemia

11111 11111 22222 22222 33333 33333 44444 44444 5501234 56789 01234 56789 01234 56789 01234 56789 01234 56789 01

H. vernalis 00000 0000? 00000 00000 00000 00000 00000 00000 010?? ?0000 00O. dilatata 00000 00000 00000 00000 00000 00000 00000 10100 01010 00??0 00X. octoculata 00000 00100 0?010 00000 01011 00000 00000 00100 10?10 00?00 00annapurna 10030 03111 11311 10131 00133 10100 01101 11111 11011 11111 01anophthalma 10000 00110 00101 10101 00011 10100 01000 10100 01000 01000 01arenicola 02222 22111 10211 10121 01023 10000 11111 11110 11010 01110 01arida 13322 22110 ?1001 10101 000?? 10100 01100 00110 11010 11000 11bedosae 10000 00110 00101 10101 00011 10100 01101 10100 11000 01000 01bellingeri 00000 20110 01001 10101 00011 10000 00000 00000 01010 01000 01brevispina 13032 03111 11311 11101 00122 10100 01101 11111 11111 11111 01buddenbrocki 10030 03111 11311 11121 00133 10100 01101 11111 11011 11111 01christianseni 13000 00110 00101 10101 00011 10100 01100 10100 01000 01000 01deharvengi 20030 03111 11311 10131 00123 11111 01101 11111 11011 11111 11delamarei 10030 0311? ???11 10121 001?? 11111 01101 11111 11??? ?1??? 01denisi 11111 11110 01001 11101 01011 10100 11101 11110 11010 11000 11dubia 10000 00110 00101 10101 00011 10100 01101 10100 01000 01000 01elisabethum 11112 11110 01001 11101 01011 10100 11101 11110 11010 11000 11fjellbergi 13322 22110 01001 10101 00011 10100 01100 00110 11?1? 11000 11granulata 10002 20110 01001 10101 00011 10100 01100 00110 11010 01000 11intermedia 13000 00110 01001 10101 00011 10100 01100 00110 11010 01000 01japonica 10022 22110 01001 10101 00011 10100 01100 10110 11010 01000 11koreana 10002 20110 00101 10101 00011 10100 01101 10100 01000 01000 01meybholae 02222 22111 11211 10131 01023 10000 11111 11110 11010 01110 11multilobata 00000 20110 0100? ?0101 00011 10000 00000 00000 01010 01000 01nadchatrami 10030 03111 11311 11101 00122 10000 01101 1111? 01111 11??1 01namibiae 00000 00110 01101 1010? 1?023 10000 01001 10100 00?10 0100? 01neocaledonica 10030 03111 11311 11121 00122 10100 01101 11111 11111 11111 01nepalensis 10030 03111 11311 10121 00122 11100 01101 11111 11011 11111 01persimilis 03002 20111 ?1201 10121 010?? 10100 11101 11110 11010 01110 01scandinavica 10002 20110 00101 10101 00011 10?00 01101 10100 01000 01000 01setonychia 20030 0311? ???11 10131 0???? 11111 01101 11111 11??? ?1??? 11similis 10000 00110 01101 10101 00011 10100 00100 10100 01000 01000 01subbulbosa 12222 22111 11201 10101 00023 10100 01100 10110 11010 01110 01trilobata 00000 00110 01101 1010? 10023 10000 01001 10100 00?10 01??? 01trisphaerae 13112 21110 01001 1?101 00011 10100 01100 00110 11010 11000 11virae 10000 00110 00101 10101 00011 10100 01101 11100 11?00 01000 01

1993). In that way, the ecological information is directlyavailable and it is almost always given on the slides
and in the literature.
RESULTS

Character State Definition

0. On antennal segment IV, apical vesicle large (0),small (1), absent (2).


1. Sensilla e1 on antennal segment IV subcylindrical(0) (Figs. 2A and 2D), candle flame-shaped (1) (Fig. 2B),globular (2) (Fig. 2C), not differentiated from ordinarysetae (3).

2. Sensilla e2 on antennal segment IV subcylindrical(0) (Figs. 2A and 2D), candle flame-shaped (1) (Fig. 2B),globular (2) (Fig. 2C), not differentiated from ordinarysetae (3).

3. Sensilla e3 on antennal segment IV subcylindrical
(0) (Fig. 2A), candle flame-shaped (1) (Fig. 2B), globular(2) (Fig. 2C), globular in cavity (3) (Fig. 2D).

FIG. 2. Antennal segments III and IV (scale bars, 0.01 mm). (A) Willemia anophthalma (right antenna, dorsal); (B) W. elisabethum (right antenna,dorsolateral); (C) W. subbulbosa (left antenna, dorsal); (D) W. deharvengi (left antenna, dorsal).

4. Sensilla d on antennal segment IV subcylindrical(0) (Figs. 2A and 2D), candle flame-shaped (1), notdifferentiated from ordinary setae (2) (Fig. 2C).

5. Sensilla i1 on antennal segment IV subcylindrical(0) (Figs. 2A and 2D), candle flame-shaped (1) (Fig.
2B), not differentiated from ordinary setae (2) (Fig. 2C).
6. Sensilla i2 on antennal segment IV subcylindrical


(0) (Fig. 2A), candle flame-shaped (1) (Fig. 2B), globular(2) (Fig. 2C), globular in cavity (3) (Fig. 2D).

7. Small internal sensilla of sensory organ of anten-nal segment III (Figs. 2A to 2D) free (0), covered inpart by a tegumental fold (1).

260 Cyrille D’Haese

8. Third and fourth antennal segments clearly sepa-rated (0), ventrally slightly fused (1).


9. Antennal segment II with 12 setae (0), 11 setae (1).10. Antennal segment I with 7 setae (0), 6 setae (1).11. Prelabral chaetotaxy with 4 setae (0), 2 setae (1).12. Labral chaetotaxy with 5.5.4 setae (0), 4.5.4 setae

(1), 2.5.4 setae (2), 5.3.4 setae (3).13. Seta a0 on the head present (0) (Fig. 1A), absent

(1) (Fig. 1B).14. Number of setae d on the head: 5 1 5 (0), 4 1 4

(1) (Figs. 1A and 1B).15. Number of setae v on the head: 2 1 2 (0), 1 1 1

(1) (Figs. 1A and 1B).16. Setae c1 on the head present (0), absent (1).17. Corneules present (0), absent (1).18. Postantennal organ with 4 to 9 vesicles (0) (Fig.

1A), 10 to 15 vesicles (1), more than 15 vesicles (2)(Fig. 1B).

19. Setae a1 of thoracic tergum III positioned on tho-racic tergum III (0), between thoracic terga II and III(1) (Figs. 1A and 1B).

20. On second and third thoracic terga, setae a1 pres-ent (0), absent (1).

21. On thoracic terga II and III, setae a2 present (0),absent (1).

22. On thoracic terga II and III, setae m3 present (0)(Fig. 1A), absent (1) (Fig. 1B).

23. Tibiotarsi I and II with 19 setae (0), 17 setae (1),12 setae (2), 11 setae (3).

24. Tibiotarsus III with 18 setae (0), 16 setae (1), 12setae (2), 11 or 10 setae (3).

25. Tibiotarsi with tenent hair (0), without tenenthair (1).

26. On thoracic tergum III, setae s (5 m7) subcylin-drical and acuminate (0), lanceolate (1).

27. On abdominal terga II and III, setae s subcylindri-cal and acuminate (0) (Fig. 1A), lanceolate (1) (Fig. 1B).

28. On abdominal tergum IV, setae s subcylindricaland acuminate (0), lanceolate (1).

29. On abdominal tergum V, setae s subcylindricaland acuminate (0), lanceolate (1).

30. On abdominal terga II and III, setae a2 present(0), absent (1).

31. On abdominal terga II and III, setae m2 present(0) (Fig. 1A), absent (1) (Fig. 1B).

32. On abdominal terga II and III, setae m3 present
(0), absent (1).
33. On abdominal terga I, II, and III, tegumentary


261

granulation normal (0), coarse secondary granulationnear setae s (1).

34. On abdominal tergum IV, setae m1 present (0)(Fig. 1A), absent (1) (Fig. 1B).

35. On abdominal tergum IV, setae m2 present (0),absent (1).

36. On abdominal tergum IV, setae m3 present (0)(Fig. 1A), absent (1) (Fig. 1B).

37. On abdominal tergum IV, setae m38 present (0),absent (1).

38. On abdominal tergum IV, setae p5 present (0)(Fig. 1A), absent (1) (Fig. 1B).

39. On abdominal tergum V, setae a3 present (0) (Fig.1A), absent (1) (Fig. 1B).

40. On abdominal tergum V, setae s in p3 position,i.e., p2 present (0) (Fig. 1A), p2 position, i.e., p2 absent(1) (Fig. 1B).

41. Ventral tube with more than 4 1 4 setae (0), with4 1 4 setae (1).

42. On abdominal sternum II, setae a3 present (0),absent (1).

43. On abdominal sternum IV, setae a1 present (0)(Fig. 3A), absent (1) (Fig. 3B).

44. On abdominal sternum IV, 4 rows of setae (0)(Fig. 3A), 3 rows of setae (1) (Fig. 3B).

45. On abdominal sternum IV, setae m1 present (0),absent (1).

46. Furca present (0), absent (1).47. On anal lobes, setae e present (0) (Fig. 4A), absent

(1) (Fig. 4B).48. On anal lobes, setae z present (0) (Fig. 4A), absent

(1) (Fig. 4B).49. On anal lobes, distal setae of hr group present

(0) (Fig. 4A), absent (1) (Fig. 4B).50. Anal spines present (0), absent (1).51. Pigmentation present (0), absent (1).

Tree Structure

Analysis of the data matrix results in two most parsi-monious trees with a tree length of 124 steps. One isidentical to the consensus, and the other differs by W.arida and W. fjellbergi clustering together. The strictconsensus is given in Fig. 5 with Bremer (1988) support
indices given at each node and synapomorphies and

ars,
FIG. 3. Chaetotaxy of abdominal sternum IV (scale b
homoplastic changes listed in Table 2. Consistency in-dex (CI) and retention index (RI) are 0.56 and 0.86, re-spectively.

According to the cladogram, the genus Willemia ismonophyletic (node 1, Fig. 5) with respect to the chosenoutgroups. This monophyly is supported by eight sy-napomorphies: antennal segments III and IV ventrallyfused (character 8: 1); head with 4 1 4 d setae (character14: 1); head with 1 1 1 v setae (character 15: 1); cor-neules absent (character 17: 1); setae a1 of thoracictergum III positioned between thoracic terga II and III(character 19: 1); tibiotarsi without tenent hair (charac-ter 25: 1); furca absent (character 46: 1); pigmentationabsent (character 51: 1).

The clade (Willemia namibiae, W. trilobata) and theclade (W. multilobata, W. bellingeri)(nodes 2 and 4, re-spectively, Fig. 5) are the earliest diverging groupswithin the genus. They are respectively characterizedby the presence of setae m38 on abdominal tergum IV

FIG. 4. Chaetotaxy of anal lobes (scale bars, 0.03


0.03 mm). (A) Willemia anophthalma; (B) W. deharvengi.

The anophthalma group as defined by D’Haese (1998)(node 6, Fig. 5) is a monophyletic group characterizedby the presence of setae a1 on abdominal sternum IV(character 43: 0). This group has a holarctic distribution(Table 3).

The denisi group is paraphyletic (Fig. 5); it is based onplesiomorphic and homoplastic characters like labralchaetotaxy with 5.5.4 setae (character 13: 0); tibiotarsiI, II, and III with 17, 17, and 16 setae, respectively(characters 23: 1 and 24: 1); setae p5 absent on abdomi-nal tergum IV (character 38: 1); on anal lobes setae eand z present (characters 47: 0 and 48: 0). These speciesshow a holarctic distribution (Table 3). However, thedenisi group redefined with W. arida, W. denisi, W. elisa-bethum, W. fjellbergi, and W. trisphaerae only is a naturalgroup characterized by sensilla e1 not differentiatedfrom ordinary setae, sensilla e2 candle flame-shaped,and setae m1 on abdominal sternum IV absent (charac-


brocki
ters 1: 3, 2: 1, and 45: 1).(character 37: 0) and setae a1 absent on thoracic terga
II and III (character 20: 1). Contrary to the previous group, the budden

mm). (A) Willemia intermedia; (B) W. wandae.

FIG. 5. Cladogram of 34 species of the genus Willemia, yielded by the analysis of the matrix in Table 1, strict consensus of two trees of 124steps, CI 5 0.56, RI 5 0.86. Bremer support indices are given above each node. Synapomorphies and homoplastic changes of nodes are listedin Table 2.

group is monophyletic (node 22, Fig. 5). The relation-ships between the species of this group are the sameas those obtained by D’Haese and Weiner (1998). Inthis latter study, the monophyly of this clade was sup-ported by three synapomorphies: sensilla e3 and i2 onantennal segment IV are large, placed in cavity, andcovered in part by tegumental fold (charaters 3: 3 and6: 3); setae m3 absent on thoracic tergum III (character22: 1). The present analysis infers four additional syna-pomorphies: labral chaetotaxy with 5.3.4 setae (charac-
ter 13: 3); setae a3 absent on abdominal tergum V (char-acter 39: 1); 3 rows of setae on abdominal sternum IV

(character 44: 1); distal setae of hr group absent on anallobes (character 49: 1). This group is represented mostlyin the oriental region, with the exception of W. bre-vispina, which is found in nearctic and neotropical re-gions, and W. buddenbrocki, which is found in bothoriental and palearctic regions (probably introduced inthe latter region) (W. Weiner personal communication)(Table 3).

Willemia subbulbosa, W. persimilis, W. arenicola, and W.meybholae form a paraphyletic group characterized by


a labral chaetotaxy with 2.5.4 setae (character 13: 2).They are known from Central and South America

30 — 18.0

Note. Character numbers correspond to character list in the text and matrix in Table 1; node numbers refer to Willemia cladogram in Fig. 5.

(Table 3). These four species with those of the budden-brocki group (node 18, Fig. 5) are a monophyletic groupbased on four synapomorphies: antennal segment IIwith 11 setae (character 9: 1); antennal segment I with6 setae (character 10: 1); setae e absent on anal lobes(character 47: 1); setae z absent on anal lobes (character48: 1).

Optimization of the Ecological Attributes

Psammophily ancestral to the genus is the most par-simonious hypothesis that fits the cladogram with 12steps (Fig. 6), whereas the alternative hypothesis,which sees psammophily as a derived feature (i.e.,
loamy habitat ancestral), requires 13 steps. If the clado-gram is constrained to retain psammophilous species

as monophyletic (W. bellingeri, W. namibiae, W. trilobataand W. arenicola, W. meybholae, and W. subbulbosa mono-phyletic, respectively), the tree is 7 steps longer thanthe most parsimonious trees (131 steps instead of 124steps). In the case of psammophily sensu lato (strictlypsammophilous species and species found in bothsandy and loamy habitats) versus strictly loam-dwell-ing species, psammophily ancestral costs 8 steps (Fig.7) while loam-dwelling life ancestral to the genus costs10 steps. If the cladogram is constrained to retain psam-mophilous species sensu lato as monophyletic (W. bel-lingeri, W. multilobata, W. namibiae, W. trilobata, W. sim-ilis, W. intermedia and W. arenicola, W. meybholae, W.persimilis, and W. subbulbosa monophyletic, respec-tively), the tree is 11 steps longer than the most parsi-


TABLE 2

Synapomorphies and Homoplastic Changes Listed by Nodes for the Willemia Cladogram in Fig. 5

Nodes Synapomorphies Homoplastic changes

1 Genus Willemia 8.1, 14.1, 15.1, 17.1, 19.1, 25.1, 46.1, 51.1 11.12 — 5.2, 37.03 — 12.1, 31.1, 35.14 20.1 23.2, 24.3, 34.1, 41.05 — 0.1, 27.1, 32.16 anophthalma group 43.0 —7 — 11.08 — 34.19 — 40.1

10 — 4.2, 5.211 38.1 12.0, 35.0, 40.112 — 4.2, 5.2, 50.113 — 1.2, 3.214 denisi group s.str. — 1.3, 2.1, 45.115 2.1, 3.1, 6.1 —16 1.1, 5.1 16.1, 21.1, 30.1, 34.1, 35.1, 36.117 — 6.2, 35.118 9.1, 10.1, 47.1, 48.1 12.2, 23.2, 24.3, 50.019 — 18.1, 34.1, 36.120 — 0.0, 21.1, 30.121 33.1 1.2, 2.2, 13.1, 27.022 buddenbrocki group 3.3, 6.3, 12.3, 22.1, 39.1, 44.1, 49.1 1.0, 4.0, 5.0, 13.1, 45.123 — 26.124 28.1, 29.1 —25 0.2 18.2, 50.126 — 23.327 — 16.128 42.1 —29 — 23.2, 24.2

monious trees (135 steps instead of 124 steps). Themost parsimonious scenario assumes that ancestral

habitats. Both species are sister groups of clades that

dwelling; P, psammophilous; P/L, species found in both sandy andloamy habitats; G, species found in guano.

psammophily reversed twice toward loam-confinedlife (nodes 7 and 12), and psammophily reappearedseveral times independently. Considering loamy habi-tat as ancestral assumes nine independent appearancesof psammophily. In both optimizations, psammophilyclearly occurred several times independently (e.g., inW. koreana, W. deharvengi, and W. brevispina), four timesin the first case and nine in the second. Whether psam-mophily or loam-confined life was deemed ancestral,ACCTRAN optimization shows that psammophily ap-
peared at node 18 (Figs. 6 and 7) and reversed towardloam-confined life in the buddenbrocki group (node 22),

265

whereas DELTRAN optimization assumes two appari-tions of psammophily convergently (Figs. 6 and 7, bot-tom left).

W. intermedia and W. similis are the two transitionalspecies between psammophilous species and loam-dwelling species; they are observed in the two different


TABLE 3

Distribution and Ecology in the Genus Willemia

Species Distribution Ecology

W. annapurna Or LW. anophthalma Pa, Ne LW. arenicola Ne PW. arida Ne LW. bedosae Pa LW. bellingeri Ne PW. brevispina Nt, Aft P/LW. buddenbrocki Or, Pa LW. christianseni Ne LW. deharvengi Aus, Or P/LW. delamarei Or LW. denisi Pa, Ne LW. dubia Ne LW. elisabethum Pa LW. fjellbergi Pa LW. granulata Ne LW. intermedia Pa, Ne P/LW. japonica Pa LW. koreana Pa PW. meybholae Nt PW. multilobata Pa P/LW. nadchatrami Or GW. namibiae Aft PW. neocaledonica Aus, Or LW. nepalensis Or LW. persimilis Nt P/LW. scandinavica Pa, Ne P/LW. setonychia Or LW. similis Pa, Ne P/LW. subbulbosa Nt PW. trilobata Aft PW. trisphaerae Pa LW. virae Pa LW. wandae Or L

Note. Distribution: Aft, Afrotropical; Aus, Australasian; Ne, Nearc-tic; Nt, Neotropical; Or, Oriental; Pa, Palearctic. Ecology: L, loam-

show radiations.

DISCUSSION

According to the phylogenetic tree, psammophilyclearly occurred several times independently in thehistory of the genus, contrary to widely held opinion.Hence it is not a derived attribute of a monophyleticgroup that arose once; that hypothesis cannot be heldany longer. Psammophily is much more evolutionarilylabile than it was thought. Moreover, in every kind ofoptimization, the most parsimonious scenario that fitsthe cladogram is psammophily ancestral to the genus.Also, reversions from psammophily to loam-confinedlife did occur. This means that, contrary to the law ofCope, specialized forms could reverse toward general-ized forms. Consequently specialization is not neces-sarily an evolutionary dead end.

On the contrary, the specialized condition is at thebasis of the radiation of the genus Willemia and of theanophthalma group, and, if we consider the ACCTRANoptimization, the specialized condition is also at thebasis of the radiation of the buddenbrocki group as well.Niche shifting made these evolutionary radiations pos-sible. It must be noticed that the two species betweenpsammophilous species and loam-dwelling species(i.e., W. intermedia and W. similis) are found in bothhabitats. This pattern suggests that some psammophi-lous species broadened their ecological niche to loamyhabitats and then lost the ability to cope with sandyhabitats conditions.

According to Mayr, “most adaptative radiations wereapparently caused by behavioral shifts” (1982: 612).Indeed, behavioral and ecological changes are evolu-tionary modifications that play a major role in drivingevolution (e.g., Aboitiz, 1990; Bateson, 1988; Darwin,1859; Futuyma and Moreno, 1988; Plotkin, 1988). In
particular, they could lead a taxon to specialization,even if some morphological changes are not inevitably

FIG. 6. Optimization of ecological attributes on the phylogeny of the genus Willemia; psammophily sensu stricto ancestral to the genus, 12steps (13 steps if loam-confined life ancestral). (P: psammophilous, thick line; L: loam-dwelling, thin line; P/L: found in both sandy and loamy

imo
habitats, gray line; G: found in guano, dotted line). An equally pars
observed (Futuyma and Moreno, 1988; Laurent, 1964).In the genus Willemia, no morphological changes canbe correlated with psammophily; loam-dwelling andpsammophilous species do not present significant mor-phological differences. However, with respect to theoutgroup, this genus shows regressive characteristicssuch as reduction of size, loss of furca, eyes, and pig-mentation, as well as short legs and antennae, charac-teristics that are traditionally considered to representadaptations to edaphic life (Gisin, 1943). Thibaud and
Christian (1997) considered that these morphologicalregressions are correlated with psammophily. Actually,

nious optimization (DELTRAN) is shown at the bottom left.

since Willemia species are edaphic, living in dark habi-tats, eyes and pigmentation are useless, and since theyare thriving in interstitial environment, the jumpingdevice (furca) is useless and awkward as are long legsand long antennae. Thus, these features could be con-sidered as adaptations to sandy habitats that made theradiation of the genus possible. Nevertheless, thesearguments also apply to loamy habitats; in that way,adaptations to sandy habitats could be exaptive toloamy habitats.


The results of phylogenetic analysis in the genusWillemia go against common sense and “the law of the

is psammophily sensu lato ancestral to the genus, 8 steps (10 steps if loam-confined life ancestral). (Psammophilous sensu lato, thick line; loam-nio
dwelling, thin line; found in guano, dotted line). An equally parsimo
unspecialized,” which see psammophily (a specializedecology) as a derived feature and as an evolutionarydead end. In fact, common sense approaches to charac-ter polarity are often wrong (Packer, 1997). Severalphylogenetical analyses show some of these resultscontradicting intuition and demonstrate the reverse tobe true. Futuyma acknowledged that even if special-ized species evolving from more generalized ancestorsis a general evolutionary trend, “In at least some cases,however, the reverse has occurred. For example, phylo-
genetic analysis has shown that some species of herbiv-orous insects with broad diet have evolved from more

us optimization (DELTRAN) is shown at the bottom left.

host-specific ancestors.” (Futuyma, 1998: 698) In thewell-known example in spiders, the orb web is ances-tral to cobwebs, with the latter arising several timesindependently in different spider lineages (Codding-ton, 1986a, b, 1988). In the same way, it was clearlydemonstrated that in crickets troglobic life is not oblig-atorily an evolutionary dead end and could reversetoward epigean habitat (Desutter-Grandcolas, 1993,1994, 1997). Even for parasitic modes of life that areconsidered irreversible (e.g., Noble and Noble, 1976;


FIG. 7. Optimization of ecological attributes on the phylogeny of the genus Willemia. The most parsimonious scenario that fits the cladogram

Price, 1980), a case study in the Diplomonadina showsthat reversal from parasitism toward free-living habits

268

occurred (Siddall et al., 1993); similar patterns werefound in Nematoda (Blaxter et al., 1998; Nielsen, 1998).In fact, according to these studies and the present work,specialization allows radiations and does not preventsubsequent evolution.

The occurrence of a macroevolutionary processshould not be judged on its likelihood. A pattern isneeded to understand what actually happened in eachclade. Results presented in this paper demonstrated,as did the studies of Coddington, Siddall et al., andDesutter-Grandcolas, that common sense is misleading(Packer, 1997) and that reversal is an evolutionary pro-cess more common than it was thought. Without thephylogenetic framework, it would be impossible toshow the complexity of the evolution of psammophily.Parsimony can permit one to infer nonparsimoniousevolutionary histories. These conclusions show how agood phylogenetic hypothesis is an essential prerequi-site for any comparative study. Phylogenetic system-atic principles provide estimates of relationships that

Orogastrura dilatata Cassagnau, 1954.

allow us to test scenarios of historical ecoethology.

APPENDIX 1

Material examined

Species of the Genus Willemia (withSynonyms in Parentheses)

anophthalma Group (sensu D’Haese, 1998)

W. anophthalma Borner, 1901.W. bedosae D’Haese, 1998.W. christianseni D’Haese, 1998.W. dubia Christiansen and Bellinger, 1980.W. koreana Thibaud and Lee, 1994.W. scandinavica Stach, 1949.W. similis Mills, 1934 (5 W. vashtia Wray, 1950).W. virae Kaprus’, 1997.

denisi Group (sensu Potapov, 1994)

W. arida Fjellberg, 1991.
W. denisi Mills, 1932 (5 W. aspinata Stach, 1949).W. elisabethum Weiner, 1986.

Cyrille D’Haese

W. fjellbergi Potapov, 1994.W. granulata Fjellberg, 1985.W. intermedia Mills, 1934 (5 W. barbarae Weiner, 1986).W. japonica Yosii, 1970.W. trisphaerae Potapov, 1994.

buddenbrocki Group (sensu D’Haese andWeiner, 1998)

W. annapurna D’Haese and Weiner, 1998.W. brevispina Huther, 1962 (5 W. australis Rapoport,

1962 5 W. peke Christiansen and Bellinger, 1992).W. buddenbrocki Huther, 1959.W. deharvengi D’Haese and Weiner, 1998.W. delamarei Prabhoo, 1971.W. nadchatrami Yosii, 1959.W. neocaledonica Weiner, 1991.W. nepalensis D’Haese and Weiner, 1998.W. setonychia Prabhoo, 1971.W. wandae Tamura, 1997.

Other Species

W. arenicola Palacios-Vargas and Vazquez, 1989.W. bellingeri Palacios-Vargas, 1988.W. biseta Christiansen and Bellinger, 1980 (species not

analyzed in this work; see text for further explanation).W. bulbosa Bonet, 1945 (species not analyzed in this

work; see text for further explanation).W. meybholae Palacios-Vargas, 1987.W. multilobata Gers and Deharveng, 1985.W. namibiae Thibaud and Massoud, 1988.W. persimilis Bonet, 1945.W. subbulbosa Thibaud, 1994.W. trilobata Barra, 1995.

Species of the Outgroup

Hypogastrura vernalis Carl, 1901.

Xenyllogastrura octoculata Steiner, 1955.

APPENDIX 2

Identification Key to the Species of theGenus Willemia

W. biseta Christiansen and Bellinger, 1980, and W.bulbosa Bonet, 1945, are not included in the key.


1. Setae a0 present on the head .............................. 2—Setae a0 absent on the head .............................. 23

2. Setae a1 present on abdominal sternum IV, labrumwith 4, 5, 4 setae, antennal segment IV with subcylin-drical sensilla; setae a0 and c1 present on head; postan-tennal organ with 5 to 12 vesicles—anophthalmagroup ............................................................................... 3

—Setae a1 absent on abdominal sternum IV ..... 10

3. Abdominal tergum V with setae s in p2 position(i.e., setae p2 absent) ..................................................... 4

—Abdominal tergum V with setae s in p3 position(i.e., setae p2 present) .................................................... 5

4. Setae a4 present on thoracic terga II and III, setaem4 present on abdominal tergum IV ............................................................................... W. bedosae D’Haese, 1998

—Setae a4 absent on thoracic terga II and III, m rowabsent on abdominal tergum IV ............................................................................................ W. virae Kaprus’, 1997

5. Setae m1 present on abdominal tergum IV ...... 6—Setae m1 absent on abdominal tergum IV ........ 8

6. Setae m3 absent on abdominal terga II and III, 3hr setae on anal lobes ................................................... 7

—Setae m3 present on abdominal terga II and III, 2hr setae on anal lobes, postantennal organ usually with5 vesicles (4 to 6). .......... W. anophthalma Borner, 1901

7. Sensilla e1 present on antennal segment IV, 2prelabral setae .............................. W similis Mills, 1934

—Sensilla e1 absent (i.e., e1 not differentiated fromordinary setae) on antennal segment IV, 4 prelabralsetae .............................. W. christianseni D’Haese, 1998

8. Sensilla d and i1 absent (i.e., d and i1 not differ-entiated from ordinary setae) on antennal segmentIV ...................................................................................... 9

—Sensilla d and i1 present on antennal segment IV.................... W. dubia Christiansen and Bellinger, 1980

9. Empodial appendage present ............................................................................... W. scandinavica Stach, 1949

—Empodial appendage absent ..................................................................... W. koreana Thibaud and Lee, 1994

10. Ventral tube with 5 1 5 setae, all tibiotarsi with11 or 12 setae ................................................................ 11

—Ventral tube with 4 1 4 setae, all tibiotarsi withmore than 12 setae ...................................................... 12


269

11. Postantennal organ with 3 vesicles, tibiotarsi IIIwith 11 setae ............................ W. trilobata Barra, 1995

—Postantennal organ with 4 vesicles, tibiotarsi IIIwith 12 setae ............................................................................................. W. namibiae Thibaud and Massoud, 1988

12. Anal spines present .......................................... 13—Anal spines absent, postantennal organ with 4 ves-

icles ................................................................................ 17

13. Abdominal tergum V with setae s in p3 position(i.e., setae p2 present) .................................................. 14

—Abdominal tergum V with setae s in p2 position(i.e., setae p2 absent) ................................................... 15

14. Postantennal organ with 4 vesicles, postantennalorgan’s vesicles blackberry-shaped, apical vesicle sim-ple .............. W. multilobata Gers and Deharveng, 1985

—Postantennal organ with 6 to 8 vesicles, postanten-nal organ’s vesicles smooth, apical vesicle trilobate ..................................... W. bellingeri Palacios-Vargas, 1988

15. Postantennal organ with 4 vesicles ....................................................................... W. intermedia Mills, 1934

—Postantennal organ with 7 vesicles or more .. 16

16. Setae a2 absent on abdominal terga II and III,setae m1 and m3 absent on abdominal tergum IV, tibio-tarsi I, II, and III with 14, 14, and 13 setae, respectively................................................... W. persimilis Bonet, 1945

—Setae a2 present on abdominal terga II and III,setae m1 and m3 present on abdominal tergum IV,tibiotarsi I, II, and III with 12, 12, and 11 setae, respec-tively ................................ W. subbulbosa Thibaud, 1994

17. Sensilla on antennal segment IV, all thick andsubcylindrical, postantennal organ’s vesicles with nu-merous secondary tubercles .......................................................................................... W. granulata Fjellberg, 1985

—Sensilla on antennal segment IV, with anothershape .............................................................................. 18

18. Setae a2 absent on abdominal terga II and III,sensilla i1 present on antennal segment IV and somesensilla are candle flame-shaped .............................. 19

—Setae a2 present on abdominal terga II and III,sensilla d and i1 absent on antennal segment IV (i.e.,d and i 1 not differentiated from ordinary setae) .. 20

19. Sensilla d present on antennal segment IV ........
.......................................................... W. denisi Mills, 1932
—Sensilla d absent on antennal segment IV (i.e., d

s 5 m7 on thoracic tergum III lanceolate ......................................................................... W. wandae Tamura, 1997

270

not differentiated from ordinary setae) ...................................................................... W. elisabethum Weiner, 1986

20. 3 sensilla (e2, e3, and i2) are candle flame-shapedon antennal segment IV W. trisphaerae Potapov, 1994

—2 sensilla (e3 and i2) are globular on antennal seg-ment IV .......................................................................... 21

21. Postantennal organ’s vesicles with numeroussecondary tubercles ................ W. arida Fjellberg, 1991

—Postantennal organ’s vesicles smooth ............. 22

22. Setae m2 present on abdominal tergum IV, setaes lanceolate on abdominal tergum I ............................................................................... W. fjellbergi Potapov, 1994

—Setae m2 absent on abdominal tergum IV, setaes subcylindrical with acuminate apex on abdominaltergum I ...................................... W. japonica Yosii, 1970

23. Sensilla e3 and i2 of antennal segment IV aresmall, globular, not placed in cavity, and not coveredby tegumental fold, setae m3 present on thoracic ter-gum III, 3 hr setae on anal lobes .............................. 24

—Sensilla e3 and i2 of antennal segment IV are large,globular, placed in cavity, and covered in part by tegu-mental fold, setae m3 absent on thoracic tergum III, 2hr setae on anal lobes

—buddenbrocki group ............................................... 25

24. Anal spines present, postantennal organ with 10to 15 vesicles ................................................................................ W. arenicola Palacios-Vargas and Vazquez, 1989

—Anal spines absent, postantennal organ with 15vesicles or more ... W. meybholae Palacios-Vargas, 1987

25. Abdominal tergum V with setae s in p2 position,313 setae on thoracic tergum I ................................. 26

—Abdominal tergum V with setae s in p3 position,212 setae on thoracic tergum I, curved and crenellatedsetae, m1 absent on abdominal sternum IV ................................................................. W. nadchatrami Yosii, 1959

26. Anal spines absent, apical vesicle absent ..... 27—Anal spines present, apical vesicle present .... 28

27. Antennal segment IV with ordinary setae, with-out lanceolate setae, postantennal organ with 18 to 20vesicles .............................. W. setonychia Prabhoo, 1971

—Antennal segment IV with ordinary setae and two
lanceolate setae, postantennal organ with 15 to 17 vesi-cles .............. W. deharvengi D’Haese and Weiner, 1998

Cyrille D’Haese

28. Abdominal terga IV and V with setae s subcylin-drical and acuminate .................................................. 29

—Abdominal terga IV and V with setae s lanceolate,postantennal organ with 8 to 12 vesicles .................................................................... W. delamarei Prabhoo, 1971

29. All tibiotarsi with 12 setae .............................. 30—Tibiotarsi I and II with 11 setae, tibiotarsi III with

11 or 10 setae ................................................................ 32

30. Thoracic tergum III with setae s 5 m7 subcylin-drical and acuminate, antennal segment IV with two orfour subcylindrical sensilla clearly differentiated fromordinary setae ............................................................... 31

—Thoracic tergum III with setae s 5 m7 lanceolate,antennal segment IV with four subcylindrical sensiliahardly distinguishable from ordinary setae ........................................ W. nepalensis D’Haese and Weiner, 1998

31. Antennal segment IV with two subcylindricalsensilla, postantennal organ with 7 to 10 vesicles ..................................................... W. brevispina Huther, 1962

—Antennal segment IV with four subcylindrical sen-silla, postantennal organ with 10 to 15 vesicles .................................................... W. neocaledonica Weiner, 1991

32. Postantennal organ with 12 to 14 vesicles, setaec1 absent on the head ................................................. 33

—Postantennal organ with about 20 vesicles, setaec1 present on the head ........................................................................... W. annapurna D’Haese and Weiner, 1998

33. Setae a3 present on abdominal sterna II and IV,setae s 5 m7 on thoracic tergum III subcylindrical ............................................... W. buddenbrocki Huther, 1959

—Seta a3 absent on abdominal sterna II and IV, setae

ACKNOWLEDGMENTS

I express my gratitude to Laure Desutter-Grandcolas, PhilippeGrandcolas, Judith Najt, and Wanda Weiner for reading the earlierdraft of the paper and providing many insightful comments, andto Jean-Francois Ponge for providing useful information about soilbiology. I thank Kathleen Reid Zeiders of Illinois Natural HistorySurvey of Champaign, Robert L. Blinn of North Carolina State Uni-
versity of Raleigh, and Michael S. Kelley of the Museum of Compara-tive Zoology of Harvard for providing type material, as well as K.


Christiansen, L. Deharveng, A. Fjellberg, J. Palacios-Vargas, and W.
Weiner, who have made material available for my work. Finally, Ithank the three reviewers for suggesting valuable improvements to the manuscript.
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