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Ecological Niche Evolution and Its Relation To 514 G. Shenbrot Сборник трудов Зоологического музея МГУ им. М.В. Ломоносова Archives of Zoological Museum of Lomonosov Moscow State University Том / Vol. 54 Cтр. / Pр. 514–540 ECOLOGICAL NICHE EVOLUTION AND ITS RELATION TO PHYLOGENY AND GEOGRAPHY: A CASE STUDY OF ARVICOLINE VOLES (RODENTIA: ARVICOLINI) Georgy Shenbrot Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev; [email protected] Relations between ecological niches, genetic distances and geographic ranges were analyzed by pair-wise comparisons of 43 species and 38 intra- specifi c phylogenetic lineages of arvicoline voles (genera Alexandromys, Chi onomys, Lasiopodomys, Microtus). The level of niche divergence was found to be positively correlated with the level of genetic divergence and negatively correlated with the level of differences in position of geographic ranges of species and intraspecifi c forms. Frequency of different types of niche evolution (divergence, convergence, equivalence) was found to depend on genetic and geographic relations of compared forms. Among the latter with allopatric distribution, divergence was less frequent and convergence more frequent between intra-specifi c genetic lineages than between either clo sely-related or distant species. Among the forms with parapatric dis- tri bution, frequency of divergence gradually increased and frequencies of both convergence and equivalence gradually decreased from intra-specifi c genetic lineages via closely related to distant species. Among species with allopatric distribution, frequencies of niche divergence, con vergence and equivalence in closely related and distant species were si milar. The results obtained allowed suggesting that the main direction of the niche evolution was their divergence that gradually increased with ti me since population split. Some initial level of niche divergence was shown to be a necessary condition providing a possibility of co-occurrence and sympatric distribution of species, whereas moderate interspecifi c co mpetition of sympatric species could be an effective driver of their further niche divergence. ЭВОЛЮЦИЯ ЭКОЛОГИЧЕСКИХ НИШ И ЕЁ СВЯЗЬ С ФИЛОГЕНИЕЙ И ГЕОГРАФИЕЙ: ИССЛЕДОВАНИЕ СЕРЫХ ПОЛЁВОК (RODENTIA: ARVICOLINI) Георгий Шенброт Взаимоотношения между экологическими нишами, генетически- ми дистанциями и положением ареалов проанализированы путём © G. Shenbrot, 2016. Ecological niche evolution in Arvicolini 515 по парных сравнений 43 видов и 38 внутривидовых филетических линий полёвок трибы Arvicolini (роды Alexandromys, Chionomys, La- siopodomys, Microtus). Показано, что уровень дивергенции ниш по- ложительно скоррелирован с уровнем генетической дивергенции и отрицательно — с уровнем различий в географическом положении ареалов видов и внутривидовых форм. Частоты различных типов эво- люции ниш (дивергенция, конвергенция, стабильность) варьируют в зависимости от уровней генетических и географических различий сравниваемых форм. Дивергенция ниш отмечена реже среди аллопа- трических форм, конвергенция ниш — чаще между внутривидовыми генетическими линиями, чем между как близко-, так и дальнерод- ственными видами. Среди парапатрических форм частота диверген- ции постепенно возрастает, а частоты конвергенции и стабильности постепенно снижаются в ряду от внутривидовых генетических линий через близкородственные виды к дальнеродственными видам. Среди аллопатрических видов частоты дивергенции, конвергенции и ста- бильности ниш у близкородственных и дальнеродственнымх видов не различаются. Полученные результаты свидетельствуют о том, что ос- новным направлением эволюции ниш является их дивергенция, уро- вень которой постепенно увеличивается со временем, прошедшим после разделения популяций. Определённый начальный уровень ди- вергенции ниш является необходимым предварительным условием, разрешающим сосуществование двух видов; межвидовая конкурен- ция умеренной интенсивности в условиях симпатрии видов может служить эффективным усилителем дальнейшей дивергенции их ниш. 1. Introduction geographic properties of species (Grinnell, Ecological niche is one of the central but 1917; Vandermeer, 1972; Whittaker et al., at the same time most controversial concepts 1973; James et al., 1984; Soberon, 2007). in current ecology. Originally, the niche was The Eltonian niche is defi ned by biotic in- considered as an attribute of the environment teractions and resource variables at a lo- but later, after Hutchinson’s (1957) intro- cal (intra-community) scale (Elton, 1927; duction of the concept of multidimensional MacArthur, 1968; Vandermeer, 1972; Lei- hyperspace of niche variables, the niche defi - bold, 1995; Soberon, 2007). nitions progressively shifted to undestanding Hutchinson (1957) had introduced an niche as an attribute of population (or spe- idea of recognition of fundamental and re- cies) in relation to its environment (Colwell, alized niches, and this became widely ac- 1992). Two aspects of the niche concept are cepted by later authors. Fundamental niche usually distinguished based on the original was defi ned as “pre-interactive” describing defi nitions, Grinnellian and Eltonian niches. potential distribution of a species (popula- The Grinnelian niche (sometime referred to tion) in multi-dimensional ecological space as habitat or ecotope, see Whittaker et al., limited by the species’ eco-physiological 1973) is defi ned by environmental variables tolerances. Realized niche was defi ned as on a broad (geographic) scale, relevant to “post-interactive” describing actual distri- understanding coarse-scale ecological and bution of a species (population) in multi-di- 516 G. Shenbrot mensional ecological space in the presence due to intra-specifi c niche differentiation and of its competitors. Pulliam (2000) expanded geographic changes in environmental con- the concept of realized niche by including ditions (James et al., 1984; Peterson, Holt, the infl uences of dispersal limitation and 2003; Devictor et al., 2010). source-sink dynamics (together with inter- The ecological niche can be characterized specifi c competition) in it. He demonstrated by two parameters, the mean (niche position that the realized niche can be narrower or or centroid) and the variance of the resource wider than the fundamental niche, depending use (niche breadth or width) (Hutchinson, on the combination of acting forces. Vander- 1957; Vandermeer, 1972). Theoretical mo- meer (1972) defi ned the Grinnellian niche as dels of niche evolution consider the both, pre-interactive (fundamental) and the Elto- i. e., evolution of niche width and niche shifts nian niche as post-interactive (realized), but (Roughgarden, 1972; Holt, Gaines, 1992; Soberon (2007) insisted on application of the Ackermann, Doebeli, 2004; Kawecki, 2008), concepts of fundamental and realized nich- whereas most empirical studies of niche evo- es to both Grinnellian and Eltonian niches. lution concentrate on shifts of niche centroids The ecological niche describes eco-physi- (Pearmanet al., 2008). ological aspects of the phenotypes of a pop- The usual method of estimation of niche ulation (Colwell, 1992). Each population divergence is measuring niche overlap us- contains a variety of ecologically specialized ing values of environmental variables in the phenotypes, and individuals of each pheno- points of occurrence of compared species, type have maximal fi tness within a specifi c either directly or through comparison of part of a resource axis present in the envi- species distribution models (SDM) (War- ronment (Roughgarden, 1972). Consequent- ren et al., 2008; Broennimann et al., 2012). ly, the shaping of niche characteristics can However, environmental data are usually be viewed as an evolutionary phenomenon spatially auto-correlated, and differences (Knouft et al., 2006). Niche evolution at- in the values of environmental variables tracted increasing attention in the theoretical between any two sets of points should literature (Roughgarden, 1972; Holt, Gaines, increase with geographic distance, thus 1992; Holt, 1996; Proulx, 1999; Ackermann, over-estimating the true niche divergence. Doebeli, 2004), especially in relation to the The tests revealed signifi cant niche differ- problem of niche conservatism (Peterson entiation in the cases, in which background et al., 1999; Graham et al., 2004; Knouft et conditions were non-overlapping, though al., 2006; Pearman et al., 2008; Warren et such conditions cannot be used as true ev- al., 2008). Most publications on this subject idence of niche differentiation (Peterson are devoted to comparison of niches among 2011). To avoid the confounding effect of species of different phylogenetic relatedness. environmental spatial auto-correlation, it It is well-known that analysis of in- is necessary to compare the observed niche tra-specifi c geographic variation is a pow- differences with the differences in back- erful tool in evolutionary studies (Mayr, ground environments (McCormack et al., 1965), however, analyzes of intra-specifi c 2009). Another problem of using the niche geographic variation of niche attributes are overlap measure for niche divergence esti- rare. At the same time, it was demonstrated mation is its inability to distinguish between that species’ ecological niches, both funda- differences in the level of divergence for mental and realized, can vary geographically non-overlapping niches. Ecological niche evolution in Arvicolini 517 Peterson et al. (1999) hypothesized that duced an idea that the niche divergence is ecological niches evolve little
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