Conservatism of Ecological
Niches in Evolutionary Time

A. T. Peterson,1* J. Soberón, 2 V. Sánchez-Cordero3
Theory predicts tow niche differentiation between species over evolutionary time scales, but little empirical evidence is available. Reciprocal geographic predictions based on ecological niche models of sister taxon pairs of birds, mammals, and butterflies in southern Mexico indicate niche conservatism over several million years of independent evolution (between putative sister taxon pairs) but little conservatism at the level of families. Niche conservatism over such time scales indicates that speciation takes place in geographic, not ecological, dimensions and that ecological differences evolve later.
Critical characteristics of species' biology, such as physiology, feeding ecology, and reproductive behavior., define their fundamental ecological niches (1). In the early1990s, several theoretical community ecologists independently predicted that fundamental niches of species under natural selection could change, but slowly. Based on diverse models 
 
 
1Natural History Museum, The University of Kansas, Lawrence, KS 66045, USA. 2Instituto de Ecología, Universidad Nacional Autónoma de México, México, D.F. 04510, México. 3Departamento de Zoología Instituto de Biología Universidad Nacional Autónoma de México, México, D.F. 04510, México.

*To whom correspondence should be addressed. Email: town@ukans.edu
that coupled population and genetic dynamics In heterogeneous environments, niche conservatism was predicted, because rates of adaptation in environments outside of the fundamental niche would often be slower than the extinction process (2).
However, little empirical evidence has been assembled to address these theoretical predictions (3). One study (4) that compared population response surfaces to climatic conditions in two closely related species of beeches (Fagus spp.) showed that limiting conditions for the presence of populations were coincident. Another study (5) documented conservatism in geographic range size in disjunct Asian and North American plant taxa, but focused principally

 
on distributional area as opposed to ecological niche characteristics. Other recent studies, however. have revealed rapid (over about 100 years) niche evolution that may be linked to speciation (6). These two contrasting views remain to be tested in broad samples of taxa to assess the generality of niche conservatism on evolutionary time scales.

We now apply new tools and approaches to examine this question in birds. mammals, and butterflies in an arena of active speciation and population differentiation -the Isthmus of Tehuantepec in southern Mexico (7). Drawing on extensive databases that summarize scientific specimen holdings, we examined 21 sister taxon pairs of birds, 11 sister taxon pairs of mammals, and 5 sister taxon pairs of butterflies and tested the degree to which ecological characteristics

 of one taxon were able to predict (with algorithm) the geographic distribution of its putative sister taxon and viceversa To provide comparisons over longer time scales, we also analyzed randomly chosen confamilial nonsister taxa (8-11).

Based on large-scale ecological dimensions, the approach uses a genetic algorithm to produce a set of decision rules in ecological space (a model of the fundamental niche) that can be projected onto map to predict potential geographic distributions. Modeling each member of the putative sister taxon pairs in this study yield not just a predicted geographic range approximating its own geographic distribution but also a predicted range mirroring the geographic distribution of its allopatric sister taxon. For example, for the hummingbird

 species pair Atthis heloisa (north and west of the isthmus) and Atthis ellioti (south and east of tlie is thmus), the model for A. heloisa successfully predicted all six occurrence points available for A. ellioti, and the model for A. ellioti predicted 66 of 79 occurrence points for A. heloisa (Fig. IA). Statistical significance of the Atthis comparisons was clear, with probabilities at about 0.03 for the first comparison and at about 10-22 for the second. Across the 37 pairs, 32 eastern taxa predicted distributions of western taxa significantly, and 26 western taxa predicted distributions of eastern taxa significantly (Fig. 1). When we examined significant and nonsignificant predictive models, we noted a strong relationship with sample size: models were nonsignificant only at sample sizes of <15 points for the predicted taxon (Fig. 2). For all taxon pairs, at least one of the reciprocal predictions was statistically significant.
 
 

 
 
 
When we compared the ability of each taxon to predict its sister taxon's distribution with its ability to predict the distributions of all other taxa, on the opposite side of the Isthmus of Tehuantepec, the difference was marked and statistically significant (12). In contrast, only a few predictions of distributions of confamilial taxa were statistically significant regardless of' sample size (Fig. 2).

The above analyses show conservative evolution in ecological niches of 37 sister taxon pairs of birds, mammals, and butterflies isolated on either side of the lowland barrier Isthmus of Tehuantepec. The forested tats on either side of' tlie isthmus have been isolated for 2.4 to 10 X 106 years (13); hence, the observed conservatism has held for effectively twice that time of independent evolution in the pairs of lineages involved. Although ages of "families" are disputed (14), this expanded time scale (perhaps 10 to 50 X 106 years) has been sufficient to permit evolutionary diversification in niche characteristics. Hence. our results broadly confirm theoretical predictions of relative conservatism in ecological characteristics of species.

Conservatism of ecological niches across moderate periods of evolutionary time also reflects the modes of speciation involved. Strict vicariant speciation depends simply on geographic isolation, whereas other scenarios, such as the peripheral isolates model of speciation and many models of sympatric speciation (15), invoke invasion of novel ecological situations as part of the speciation process. The taxa and ecological dimensions treated here support the 

 hypothesis with ecological differences building up later, well after the speciation event. An untested question is whether the observed conservatism results from active constraint (stabilizing selection) or whether it reflects tlie absence of additive genetic variation in niche-related traits (16). Similarly, our analysis does not eliminate the possibility of niches of' both members of species pairs responding in parallel to broad-scale environmental changes.

To the extent that our geographic scenario is representative, our results suggest that ecological niches evolve little at or around the time of the speciation event. Rather, ecological niche differences appear to accumulate later, over the time scale of familial relationships. Finding general conservatism in ecological niches opens the door to phylogenetic studies of niche evolution, comparative evaluations of conditions under which niche conservatism breaks down, construction of predictive distributional models. and numerous other applications to questions in biogeography (estimates of a and b diversify, centers of endemism), biodiversity (foci of species diversity), and conservation biology (development of conservation prioritizations).

References and Notes

1. M. L. Rosenzweig, Evol. Ecol. 1, 315.

2. R. D. Holt and M. S. Gaines, ibid. 6, 433 (1992); J. S. Brown and N. B. Pavlovic, ibid., p. 360; A. 1. Houston and J. M. McNamara, ibid., p. 243; T. J. Kawecki and S. C. Stearns, ibid. 7, 155 (1993).

3. H. H. Ross, Taxon 21, 253 (1972); A. J. Boucot, J. Paleontol. 57, 1.

4. B. Huntley, P. J. Bartlein, 1. C. Prentice, J. Biogeogr. 16, 551 (1989).

5, R, E. Ricklefts and R. E. Latham, Am. Nat. 139, 1305 (1992).
 

 6. M. R. Orr and T. B. Smith, Trends Ecol. Evol. 13, 502 (1998).

7. T. P. Ramamoorthy et al., Biological Diversity of Mexico: Origins and Distribution (Oxford Univ. Press, New York, 1993).

8. We obtained distributional data for the bird, mammal, and butterfly species or distinct subspecies involved from label data on specimens in the systematic collections cited in A. T. Peterson et al. [Ibis 140, 288, (1998)] and J. E. Llorente-Bousquets et al. [Papilonidae y Pieridae de México: Distribución Geográfica e Ilustración, Universidad Nacional Autónoma de México, México (1997)] as well as thc mammal collection of the University of Kansas Natural History Museum and thc Colección Nacional de Mamíferos, Instituto de Biología Universidad Nacional Autónoma de México. Species pairs were selected according to the following criteria: (1) that they constitute clear examples of sister taxa phylogenetically (for example, the only two species in a genus or the only two well-marked subspecies in a species); (2) that they are separated by the Isthmus of Tehuantepec (with the minor exception of taxon pairs with distinct migratory and resident populations); (3) that distributions of both taxa abut the isthmus fairly directly; and (4) that sample sizes available are sufficient to permit testing.

9.The following species pairs and confamilial species were included. Birds: Accipiter striatus + Accipiter chionogaster, Buteo nitidus; Amazilia beryllina + Amazilia devillei, Heliomaster longirostris; A. heloisa + A. ellioti, Hylocharis eliciae; Chlorostilbon canivetii + Chlorostilbon salvini, Tilmatura dupontii; Colaptes cafer + Colaptes mexicanoides, Melanerpes uropygialis; Cyanocitta, coronata + Cyanocitta ridgwayi, Cyanocorax beecheii; Cyrtonyx montezuma + Cyrtonyx ocellatus, Colinus virginianus; Doricha eliza + Doricha, sp. nov. (A. T. Peterson et al., unpublished data), Campylopterus excellens; Empidonax occidentalis + Empidonax flavescens, Camptostoma imberbe; Ergaticus ruber I Ergaticus versicolor, Pipilo chlorurus; Eugenes fulgens + Eugenes viridiceps, Campylopterus hemileucurus; Falco sparverius + Falco tropicalis, Falco mexicanus, Icterus pustulatus + Icterus sclateri, Pheucticus melanocephalus; Melanotis caerulescens + Melanotis hypoleucum, Toxostoma redivivum; Mimus polyglottos + Mimus gilvus, Toxostoma bendirei; Pheucticus chrysopeplus + Pheucticus aurantiacus, Lanio aurantius; Picoides jardinii + Pocoides sanctorum, Picoides scalaris; Salpinctes obsoletus - Salpinctes neglectus, Thryothorus maculipectus; Sayornis nigricans + Sayornis acuatica, Mionectes oleagineus; Strix varia + Strix fulvescens, Glaucidium gnoma; and Turdus assimilis + Turdus leucachen, Turdus infuscatus. Mammals: Sorex oreopolus Sorex sclateri, Megasorex gigas; Sorex oreopolus + S. stizodon, Sorex milleri; Artibeus aztecas aztecus + Artibeus aztecas minor, Chrotopterus auritus; Dasyprocta mexicana + Dasyprocta punctata (no other confamilial species are available in 

 
Mexico); Habromys lepturus + Habromys lophurus, Neotoma goldmani; Microtus oaxacensis + Microtus guatemalensis, Peromyscus polius; Microtus umbrosus + Microtus guatemalensis, Peromyscus melanophrys; Peromyscus melanocarpus + Peromyscus zarhynchus, Tylomys nudicaudus; Peromyscus megalops + Peromyscus zarhynchus, Peromyscus merriami; and Sciurus colliaei + Sciurus yucatanensis, Ammospermophilus leucurus. Butterflies: Catasticta nimbice nimbice + Catasticta nimbice ochracea, Leptophobia aripa; Dismorphia eunoe eunoe + Dismorphia eunoe chamula, Dismorphia amphione; Pereute charops charops + Pereute charops nigricans, Pyrisitia proterpia; Pereute charops leonllae + Pereute charops nigricans, Ascia monuste; and Pyrrhosticta abderus abderus + Pyrrhosticta abderus electryon, Battus eracon. Species names and taxonomic arrangements followed the American Ornithologists' Union (Check-list of North American Birds , American Ornithologists' Union, Washington, DC, ed. 7, 1998) and A. T. Peterson and A. G. Navarro (unpublished data) for birds, D. E. Wilson and Reeder (Mammal Species of the World, Smithsonian Institution Press, Washington, DC, ed. 2, 1993) for mammals, Tyler et al. (Swallowtail Butterflies of the Americas, Gainesville Scientific Publishers, Gainesville, FL, 1994) for Papilionidae, and 1. Vargas et at. (J. Lept. Soc. 50, 97, 1996) for Pieridae.

10. Locality data were georeferenced to the nearest 10 3 degree and reduced to unique latitude-longitude combinations for each species. The four thematic geographic coverages used (annual mean temperature, annual mean precipitation, elevation, and potential vegetation) consisted of raster grids (7 X 7 km pixels) available from the Comisión Nacional para el Uso y Conocimiento de la Biodiversidad (http:// www.conabio.gob/). Geographic distributional predictions were developed based on algorithms designed to evaluate correlations between distributional occurrences and environmental characteristics (niches). The Biodiversity Species Workshop facility developed by David Stockwell (http://biodi.sdsc.edu/) provides an implementation of the Genetic Algorithm for Rule-Set Prediction [GARP; D. R. B. Stockwell and 1. R. Noble, Math. Comp. Simul. 33, 385, (1992); D. R. B. Stockwell and D. Peters, Int. J. Geogr. Inf, Sci. 13, 143 (1999)]. GARP works in an iterative process of rule selection, evaluation, testing, and incorporation or rejection: first, a method is chosen from a set of possibilities (logistic regression, bioclimatic rules), and then it is applied to the data and a rule is developed. Predictive accuracy is then evaluated based on 1250 points resampled from the test data set and 1250 points sampled randomly from the study region as a whole. The change in predictive accuracy from one teration to the next is used to evaluate whether a particular rule should be incorporated into the model. The algorithm runs either 1000 iterations or until convergence. 

 Distributional predictions from GARP may often include areas not inhabited, an effect of the modeling being focused on ecological niches instead of geographic distributions; these commission errors in some cases may be reduced by inclusion of additional ecological dimensions or may require consideration of historical factors that lead to the absence of species from habitable areas.
11. A x2 statistic was used to evaluate statistical significance of reciprocal predictions of taxa, with expected numbers based on points for the predicted taxon that would fall within the area predicted present if distributed randomly. Reciprocal tests were conducted for each taxon pair. To evaluate relative degrees of conservatism of ecological niches of sister taxa, we compared the reciprocally predictive accuracy of sister taxon pairs with that for randomly chosen nonsister taxa within the same family. Statistical significance of these comparisons was evaluated by using ecological models for the sister taxon pair to predict the distribution of the nonsister taxon and tested by overlay of the points available for that species by using the X2 approach described above.

12. A median test comparing prediction of sister taxa with that for all other taxa included in the study from a particular side of the isthmus: eastern form predicting western form, X2 = 6.31, degrees of freedom (df) = 1, P = 0.012; western predicting eastern, x2 = 5.10, df = 1, P =- 0.0239.

13. T. Wendt, Anales Inst. Biol. UNAM 58, 29 (1989); A. Graham, in Biological Diversity of Mexico: Origins and Distribution, T. P. Ramamoorthy et al., Eds. (Oxford Univ. Press, New York, 1993), p. 109.

14. A. Cooper and D. Penny, Science 275, 1109 (1997); T. Stidham, Nature 396, 29 (1998).

15. D. J. Futuyma, Evolutionary Biology (Sinauer Associates, Sunderland, MA, ed. 3, 1997); E. Mayr, Animal Species and Evolution (Harvard Univ. Press, Cambridge, MA, 1963).

16. A. D. Bradshaw, Philos. Trans. R. Soc. London Ser. B 333, 289 (1991).

17. Supported by the National Science Foundation, Kansas EPSCor, Dirección General de Asuntos del Personal Académico de la Universidad Nacional Autónoma de México, Consejo Nacional de Ciencia y Tecnología, and the National Geographic Society. We thank the Comisión para el Uso y Conocimiento de la Biodiversidad for making geographic coverages available; the curators of scientific collections for providing access to species occurrence data; R. Holt and E. Wiley for discussions; and A. Navarro Sigüenza, J. Llorente Bousquets, D. R. B. Stockwell, R. M. Timm, and H. Benitez Diaz for assistance and access to data.
 
www.sciencemag.org
27 January 1999; accepted 7 July 1999
SCIENCE VOL 285 20 AUGUST 1999 PAGES 1265-1267