The concept of species and practical : what is in-between?

The concept of species and practical taxonomy: what is in-between?

Rimantas Rakauskas The ecological approach considers the biological species as an ecological unit. This does not exclude recognition of biological species also as a Vilnius University, genetic and morphological (sensu lato) unit. The article deals with the M. K. Èiurlionio 21/27, theoretical and practical aspects of such a treatment of the concept of LT-2009 Vilnius, Lithuania. biological species on the examples of (, Sternorrhyncha: E-mail: [email protected] ) taxonomy. Key words: species concepts, taxonomy,

INTRODUCTION performed by the species in nature. The following features seem to be characteristic of the biological “Since the species are the units of evolution, and since species therefore. they are the base units of biological systematics, a 1. A species is an ecological unit. A species is a proper understanding of species is crucial for the suc- system of related populations that are similarly adap- cess of evolutionary biology and biological systema- ted (Shaposhnikov, 1981; Blackman, 1995). All popu- tics” (Ereshefski, 1992). Such or similar statements lations of the species have specific adaptations for sur- seem to be generally accepted among biologists. That viving in the ecological niche of that species, and every is not the case when considering what the species re- population may have populational adaptations for sur- ally is. Numerous concepts and definitions of species viving in its particular ecological subniche. Therefore are available, and none of them is widely accepted the species is to be treated as an ecological unit. Spe- (Blackman, 1995; Grant, 1963; Klimaszewski et al., cies-specific adaptations are responsible for the speci- 1995; Mayr 1963; 1976; 1982; Matile et al., 1993; fic role performed by a particular species in nature. Çàâàäñêèé, 1968). Several papers appeared, propaga- 2. A species is a genetic unit. Species-specific adap- ting the understanding of biological species as an eco- tations must be fixed and inherited genetically. Thus, logical unit, particularly addressing the aphid (Hemi- ecological specificity of the species is underlain by the ptera, Sternorrhyncha: Aphididae) taxonomy (Shaposh- genetic specificity. Forces responsible for the specifi- nikov, 1981; 1987; Rakauskas, 1998). The aim of the city and unity of the gene pool of the species are present paper is to discuss such understanding of spe- interpopulational gene flows (Dobzhansky, 1970; Ma- cies from the point of view of practical taxonomic yr, 1982), specific mate recognition systems (Paterson, procedures, based on the examples from aphid biosys- 1993), common selective regimes (Ehrlich et al., 1992). tematic studies. Selection might be treated as the most general force of maintaining or disturbing the unity of the gene pool of BIOLOGICAL SPECIES AS AN ECOLOGICAL UNIT a particular species. 3. A species is a morphological (sensu lato) unit. Ecological methodology in the species-level taxonomy Species-specific adaptations are provided due to spe- is based on the following ideas (Rakauskas, 1997; cies-specific morphological (sensu stricto), anatomical, 1998; 2001). When describing the species as a general physiological, cytogenetic, biochemical, immunologi- biological phenomenon, a more general biological ap- cal, etc. features, the inheritance of which is underlain proach is needed. It is often quoted that “in biology by the specificity of the gene pool of the species. Spe- nothing makes sense except in the light of evolution” cies-specific adaptations need species-specific charac- (Dobzhansky, 1970: 6). On the other hand, biological ters. An important practical conclusion that follows evolution is the process of adaptation of living things from understanding this fact is that real species can be (Dobzhansky, 1970; Grant, 1963; Ridley, 1993; recognized by their morphological characters. The so- Ñåâåðöîâ, 1987). Following this, one may consider called morphological species of early taxonomists are that the main characteristic of the species is the role still valid in many cases therefore.

ISSN 0235–7224. E k o l o g i j a (Vilnius). 2003. Nr. 1

3 Rimantas Rakauskas

4. Treating species as a system of populations is ques (e. g., allozymes or DNA analysis) seem to be not useful for understanding the evolutionary processes. necessary. Cytogenetic and molecular methods are ne- The idea of the complex nature of a species consisting eded when ecological and morphological ones are in- of subspecific units having a potential to diverge (or, sufficient on their own. Anyway, purely morphologi- in other expression, forego its own evolutionary (ten- cal, cytogenetic or molecular descriptions of aphid spe- dencies) was present in Darwin’s theory, and it is still cies, without any ecological data on new taxa, should actual in population-genetic modern synthesis (Âàâè- be avoided. Information on the life cycles and host ëîâ, 1931; Dobzhansky, 1970; Mayr, 1982). There is specificity is necessary in all cases. Let us see how this no need to multiply species numbers by giving specific methodology works in practice. names to every “smallest diagnosable cluster of indi- vidual organisms” (Cracraft, 1992). It is population EXAMPLES FROM APHID TAXONOMY but not the species that is an elementary unit of evo- lution, the smallest group of individuals having a po- Aphid species of the genus Aphis L. living on currants tential of independent evolution. and gooseberries (Ribes spp.) in the Palaearctics If any name for the above-mentioned understan- ding of species is needed, such a concept of species is Four species of the genus Aphis are reported as inha- to be called “biological species”, because understanding biting currants and gooseberries (Ribes spp.) in the species as a coadapted gene pool inhabiting a certain Palaearctics: A. grossulariae Kaltenbach, 1843, A. “adaptive peak” of “adaptive landscape” was already schneideri (Börner, 1940), A. triglochinis Theobald, 1926 present in the concept of biological species (Dob- and A. popovi Mordvilko, 1932. Numerous data con- zhansky, 1970: 26). cerning host specificity, life cycles and morphological Having recognized the above-mentioned features of features are available for the first three European spe- the biological species, what are the consequences for cies (for a wider review, see Rakauskas, 1998a). The defining the species in taxonomy? When understanding fourth one is a Siberian species, closely related morpho- the biological evolution (including speciation) as the logically to the European A. schneideri; its entire life history of adaptation of living things one might con- cycle is not known (Rakauskas, 1996). When treating sider that the main feature of species is the role per- a species as an ecological unit, one can justify the formed by it in nature. That is, the main characteristic existence of three ‘good’ species inhabiting currants of the species is its ecological niche. When solving the and gooseberries in Europe: the first is holocyclic mo- problem, is it one or two species, it is necessary to noecious on Ribes spp. (A. schneideri), the second is estimate the ecological specificity of the organisms holocyclic facultatively heteroecious between Ribes spp. studied. and Onagraceae (A. grossulariae), and the third one Generally, all structural, physiological, biochemi- obligatorily alternates between Ribes spp. and various cal, etc. characters of living things serve one purpose – Brassicaceae, Boraginaceae, Asteraceae hosts (A. triglo- successful existence in certain habitats. Morphology, chinis). Nevertheless, the ecological niche of aphid spe- anatomy, physiology, cytogenetics, biochemistry, etc. cies is not easy to define precisely, its boundaries re- can provide valuable information when deciding whe- main uncertain. E. g., monoecious holocyclic clones of ther the organisms under analysis are adapted to simi- A. grossulariae have been documented (Ãóñûíèíà, lar ecological niches (they belong to the same species 1963), making this species similar to A. schneideri. Re- in such case) or to different niches (the case of diffe- suming the available information on host specificity, rent species). Excellent understanding of the charac- life cycles, phenology and parasitoid-predatory species ters studied and successful intuition may result in a composition, only A. triglochinis seems to be a “good” proper description of the species based on one or few species, whilst A. grossulariae and A. schneideri share criteria only. Morphospecies of early taxonomists are many similar features (Rakauskas, 2000). Furthermo- still valid in many cases therefore. Nevertheless, the re, successful interspecific crossing experiments were probability of mistakes in such cases is much greater performed on these species, raising the question of the than when exploiting more criteria. possibility of natural hybridisation (Rakauskas, 1999). Concerning aphids, information on the life cycle Intermediate hybrid morphotypes appeared to be not and host specificity is supposed to be absolutely neces- so rare in natural conditions (Rakauskas, 2002). Ad- sary for understanding their ecological specificity. Mor- ditional ecological and morphological studies are ne- phological analysis is necessary for a proper diagnosis eded to clarify the taxonomic status of A. popovi – it of aphid species and constructing practical identifica- might be a sibling vicariant species to the European A. tion keys. Thus, when distinct differences in life cycles schneideri in Siberia, or just a Siberian representative and host specificity correlated with clear morphologi- (subspecies?) of A. schneideri. Molecular data seem to cal specificity and biogeographical evidence are avai- be necessary for the final decision on how many spe- lable, sophisticated and expensive molecular techni- cies of Aphis live on Ribes spp. in the Palaearctics.

4 The concept of species and practical taxonomy: what is in-between?

DNA analysis techniques (e. g., Sunnucks et al., 1997) dignifying a new aphid subspecies. A formal description seem to be most promising at the moment. Relations of a new subspecies urgently emphasizes the need of between the Palaearctic and Nearctic currant-inhabi- documenting the morphological differences between the ting Aphis species also demand molecular techniques. subspecies, correlated with their ecological specificity. That is, the Nearctic A. neomexicana – oenotherae The subspecies of cerasi (F.) represent a good complex is greatly similar to the Palaearctic A. gros- example of a proper subspecies (Gruppe, 1988; Müller, sulariae in its life cycle, host specificity and morpho- 1969). That is not the case with M. knautiae, where the logy (for a wider account, see Rakauskas, 2000). DNA evidence for different life cycle and/or host specificity sequencing and subsequent phylogenetic analysis (e. g., modes, followed by distinct morphology, reproductive Goto et al., 2001) might clarify the question whether barriers and distribution peculiarities is lacking. Con- Nearctic and Palearctic currant Aphis counterparts are trary to the above example of the currantdwelling Aphis the same species (which seems likely from ecological species, molecular analysis of Macrosiphum species li- and morphological data), or they are vicariant sibling ving on Knautia in Europe is not necessary. The avai- species that converged due to similar ecological niches lable ecological, morphological and zoogeographical data being exploited on different continents. are enough to justify the existence of only two Macro- siphum species inhabiting Knautia in Europe. Aphid species of the genus Macrosiphum Pass. living These examples show the ecological understanding on Knautia spp. in Europe of biological species to be not just a theoretical const- ruction, but a useful tool for taxonomic practice as Three species of the genus Macrosiphum are reported as well. As concerns the aphid taxonomy, such understan- inhabiting Knautia spp. (Dipsacaceae) in Europe. M. ding of species emphasizes the necessity to study aphid rosae (Linnaeus, 1758) is facultatively heteroecious bet- life cycles and host specificity, followed by the morpho- ween Rosa and various Dipsacaceae, Valerianaceae and logical analysis of ecologically different aphid clones. Onagraceae hosts, the life cycle and host specificity Valuable additional information can be supported by being well documented from the very beginning of the cytogenetic, biochemical characters (allozymes and last century (for a wider review, see (Ðàêàóñêàñ è äð., DNA analysis) and hybridization experiments. Ne- 1983). M. knautiae Holman, 1972 and M. silvaticum vertheless, molecular data might appear necessary in Meier, 1985 are holocyclic monoecious on Knautia spp; certain cases. One must clearly recognise that life cycle that was proven experimentally for M. knautiae in Mo- and host specificity are not the only and maybe even ravia (Holman, 1972) and M. silvaticum in Lithuania not the most important characters of the aphid ecolo- (Ðàêàóñêàñ, 1985). These two species utilize the same gical niche. Different ecological features might indica- species of the genus Knautia, are sympatric in their te just different intraspecific units – host/life cycle distribution and resemble each other in their morpho- races or subspecies. Similar life cycle and host speci- logical features (Rakauskas, 2002). Ecological unders- ficity might be characteristic of different species (e. g., tanding of biological species suggests the existence of vicariant species that can appear due to their different two Knautia-inhabiting Macrosiphum species in Europe. zoogeographical pathways). Host plant specificity is One is M. rosae. It is facultatively heteroecious between closely dependent on the taxonomy of host plants: the Rosa and various Dipsacaceae, Valerianaceae and Onag- “same” plant species might in fact concern an aggre- raceae hosts. Another species is oligophagous on Knau- gate of different sibling plant taxa having different en- tia spp. According to the Principle of Priority (Interna- vironmental needs. For example, Knautia arvensis (L.) tional , art. 23), a valid name for this species is Macro- Coult. is sometimes treated as an aggregate of species siphum knautiae Holman, 1972, whilst Macrosiphum (Štepanek, 1997). If this would be the case, the situ- silvaticum Meier, 1985 is a younger synonym. This is ation with M. knautiae in Europe should be also re- justified, because M. knautiae and M. silvaticum have vised. So, aphidologists do not have the only, the main the same host specificity and life cycles, share a similar or the most important criterion for recognising the morphology and have the same distribution area. The species, at least nowadays. Therefore the multidiscip- idea of two subspecies inside M. knautiae (Holman, linary approach (Blackman et al., 1995) seems to be 1972) is not reasonable for the present understanding of the most relevant in taxonomic studies at present. Wha- biological species as an ecological unit and applying tever methods exploited, the taxonomic evaluation of ecological thinking also to the subspecies level (Black- data should involve their ecological interpretation. man et al., 1991; Rakauskas, 2001). Subspecies should be an ecological variant (subunit) of the species. The CONCLUSIONS main characteristic of the aphid subspecies should be its ecological specificity. The ecological specificity of a 1. Following the general methodology of ecological certain aggregate of aphids, accompanied by the genetic thinking in biology, the biological species should be and morphological specificity, is to be proven when treated as an ecological unit.

5 Rimantas Rakauskas

2. Treating the biological species as an ecological 13. International Code of Zoological Nomenclature. Fourth unit does not exclude understanding the biological spe- Edition. London: The International Trust for Zoolo- cies also as a genetic and morphological (sensu lato) gical Nomenclature. 1999. 306 p. unit. 14. Klimaszewski S., Wojciechowski W., Jedlièka L. Podsta- wy systematyki zoologicznej. Katowice: Wydawnictwo UÚ. 3. Ecological methodology stresses the need of eco- 1995. 92 p. logical analysis in taxonomical practice. The results 15. Mayr E. species and evolution. Cambridge, received when applying different methods of taxono- Mass.: Harvard University Press. 1963. 797 p. mic analysis (morphometry, ethological, immunologi- 16. Mayr E. Evolution and the diversity of Life. Cambridge, cal, physiological analysis, cytogenetic and molecular Mass.: Harvard University Press. 1976. 758 p. methods, etc.) should be evaluated in the ecological 17. Mayr E. The Growth of Biological Thought: Diversity, context, concerning the specificity of the ecological Evolution, and Inheritance. Cambridge, Mass.: Har- niche of supposed species. Direct ecological analysis is vard University Press. 1982. 974 p. 18. Matile L., Tassy P., Goujet D. Wstæp do systematyki highly appreciated. zoologicznej. Warszawa: PWN. 1993. 107 p. 4. When describing the aphid species, information 19. Müller F. P. Bastardierungsversuche zur Feststellung on the life cycles and host specificity, followed by the von Isolierungsmechanismen zwischen nahe verwand- morphological analysis of ecologically different clones, ten Formen in der Gattung Myzus passerini (Homop- is absolutely necessary. Valuable additional informa- tera: Aphididae). Biol. Zbl. 1969. Vol. 88. P. 147–164. tion can be supported by cytogenetic, biochemical cha- 20. Paterson H. Evolution and the recognition concept of racters (allozymes and DNA analysis) and hybridiza- species: collected writings. Baltimore: John Hopkins Uni- tion experiments. versity Press. 1993. 234 p. 21. Rakauskas R. Redescription of Aphis popovi and its relations with other Palaearctic species of the genus References Aphis inhabiting Ribes (Hemiptera: Aphidoidea: Aphi- 1. Blackman R. What’s in a name? Species concepts didae). Eur. J. Entomol. 1996. Vol. 93. P. 249–254. and realities. Bull. Ent. Res. 1995. Vol. 85. P. 1–4. 22. Rakauskas R. Biologinë rûðis kaip ekologinë sàvoka. 2. Blackman R. L., Brown P. A. Morphometric variation Ekologija (Vilnius). 1997. Nr. 4. P. 58–62. within and between populations of Rhopalosiphum 23. Rakauskas R. What is the (aphid) species? Nieto maidis with a discussion of the taxonomic treatment Nafria J. M. & Dixon A. F. G. (Eds.) Aphids in of permanently parthenogenetic aphids (Homoptera: natural and managed ecosystems. Leon: Universidad Aphididae). Entomologia Generalis. 1991. Vol. 16(2). de Leon. 1998. P. 447–451. P. 97–113. 24. Rakauskas R. Morphometric analysis of European 3. Blackman R., Watson G., Ready P. The identity of species of the genus Aphis (Sternorrhyncha: Aphidi- the African pine wooly aphid: a multidisciplinary ap- dae) inhabiting Ribes. Eur. J. Entomol. 1998a. Vol. 95. proach. Bulletin OEPP. 1995. Vol. 25. P. 337–341. P. 239–250. 4. Cracraft J. Species Concepts and Speciation Analy- 25. Rakauskas R. Hybridisation between Aphis grossula- sis. The Units of Evolution: Essays on the Nature of riae and Aphis schneideri (Sternorrhyncha: Aphididae): Species. 1992. P. 93–120. an experimental approach. Eur. J. Entomol. 1999. Vol. 5. Dobzhansky T. Genetics of the Evolutionary Process. 96. P. 401–408. New York: Columbia University Press. 1970. 505 p. 26. Rakauskas R. On the identity of Aphis neomexicana 6. Ehrlich P., Raven P. Differentiation of Populations. (W. P. and T. D. A. Cockerell, 1901). Aphids and other The Units of evolution: Essays on the Nature of Species. Homopterous (Warszawa). 2000. Vol. 7. P. 7–14. 1992. P. xiii. 27. Rakauskas R. Lietuvos amarø (Hemiptera, Sternorrhyn- 7. Ereshefsky M. The Units of Evolution: Essays on the cha: Aphididae) biosistematiniai tyrimai. Vilnius: VU Nature of Species. Cambridge, Mass.: The MIT Press. leidykla. 2000. 128 p. 1992. 405 p. 28. Rakauskas R. What is the (aphid) subspecies? Ma- 8. Goto S. G., Kimura M. T. Phylogenetic utility of terials of the Sixth International Symposium on Aphids. mitochondrial COI and nuclear Gpdh genes in Dro- Rennes (France), 3–7 September 2001 (in press). sophila. Molecular Phylogenetics and Evolution. 2001. 29. Rakauskas R. Natural hybridisation between Aphis Vol. 18(3). P. 404–422. grossulariae and Aphis schneideri: morphological evi- 9. Grant V. The Origin of Adaptations. New York: Co- dence (Sternorrhyncha: Aphididae). Eur. J. Entomol. lumbia University Press. 1963. 606 p. Submitted in March 2002. 10. Grant V. Evolution of the Species Concept. Biol. 30. Rakauskas R. Macrosiphum on Knautia in Europe: Zent. Bl. 1994. Vol. 113. P. 401–415. biology, morphology and systematics, including new 11. Gruppe A. Electrophoretische Untersuchungen zur synonymy (Hemiptera: Aphididae). Deutsche ent. Unterscheidung der Subspecies von Myzus cerasi F. Zeitschr. Submitted in May, 2002. (Hom., Aphididae). J. Appl. Ent. 1988. Vol. 105. 31. Ridley M. Evolution. Cambridge, Mass.: Blackwell P. 460–465. Science. 1993. 670 p. 12. Holman J. Description of Macrosiphum knautiae sp. 32. Shaposhnikov G. Populations and Species in Aphids n., with notes on the taxonomy of the M. rosae group and the Need for a Universal Species Concept. Otta- (Homoptera, Aphididae). Acta Ent. Bohemoslov. 1972. wa: Agric. Canada Res. Branch Publication. 1981. Vol. 69. 175–185. 61 p.

6 The concept of species and practical taxonomy: what is in-between?

33. Shaposhnikov G. Organisation (Structure) of Popu- äëÿ Ëèòîâñêîé ÑÑÐ âèäû íàñåêîìûõ. Ñîîá- lations and Species, and Speciation. Aphids. Their Bio- ùåíèÿ è îïèñàíèÿ 1985 ãîäà. 1985. Ñ. 9–13. logy Natural Enemies and Control, A. Amsterdam: El- 40. Ðàêàóñêàñ Ð. Ï., Çàÿí÷êàóñêàñ Ï. À. Áèî- sevier. 1987. P. 415–430. ëîãè÷åñêèå îñîáåííîñòè çåëåíîé ðîçàííîé òëè â 34. Sunnucks P., De Barro P. J., Lushai G., Maclean N., Ëèòîâñêîé ÑÑÐ. Òð. ÀÍ ËèòÑÑÐ. Ñåð. Â. Hales D. Genetic structure of an aphid studied using 1983. Ò. 2(82). Ñ. 70–78. microsatellites: cyclic parthenogenesis, differentiated 41. Ñåâåðöîâ À. Ñ. Îñíîâû òåîðèè ýâîëþöèè. Ìîñê- lineages and host specialization. Molecular Ecology. âà: Èçä-âî ÌÃÓ. 1987. 320 ñ. 1997. Vol. 6. P. 1059–1073. 35. Štepanek J. Knautia L. – chrastavec. Kvetena Èeské Rimantas Rakauskas Republiky, 5. Praha: Academia. 1997. P. 543–554. RÛÐIES KONCEPCIJOS IR PRAKTINË 36. Âàâèëîâ Í. È. Ëèííååâñêèé âèä êàê ñèñòåìà. SISTEMATIKA: KAS BENDRO? Òð. ïî ïðèêë. áîò., ãåí. è ñåë. 1931. Ò. 26(3). Ñ. 109–134. Santrauka 37. Ãóñûíèíà Ë. Ì. Òëè ðîäà Aphis L. íà Ekologinë màstysena verèia suvokti biologinæ rûðá kaip ñìîðîäèíå è êðûæîâíèêå. Òð. Áèîë. èí-òà Ñèá. ekologiná vienetà. Pastaroji rûðies samprata neprieðtarau- îòä. ÀÍ ÑÑÑÐ. 1963. Ò. 10. Ñ. 77–81. ja biologinës rûðies, kaip genetinio ir morfologinio (pla- 38. Çàâàäñêèé Ê. Ì. Âèä è âèäîîáðàçîâàíèå. èiàja prasme) vieneto, supratimui. Straipsnyje aptariami Ëåíèíãðàä: Íàóêà. 1968. 396 ñ. tokios rûðies koncepcijos teoriniai aspektai ir praktinio 39. Ðàêàóñêàñ Ð. Ï. Macrosiphum silvaticum Meier– taikymo galimybës, remiantis pavyzdþiais ið amarø (He- íîâûé äëÿ ÑÑÑÐ âèä òëåé, îáíàðóæåííûé â miptera, Sternorrhyncha: Aphididae) sistematikos. Ëèòîâñêîé ÑÑÐ â 1978–1983 ãã. Íîâûå è ðåäêèå Raktaþodþiai: rûðies koncepcija, sistematika, amarai

7