Trends Ecol Research Articles

Conservation genetics gets a textbook

DOI: 10.1016/S0168952502027889An Introduction to Conservation Geneticsby R. Frankham, J.D. Ballou and D.A. BriscoeCambridge University Press, 2002. US$50/£34.95 pbk (xiii + 617 pages) ISBN 0521639859Does conservation genetics matter in the effort to save the Earth's biodiversity? Some of the major conservation organizations don't think so and would rather focus on species inventories wholly ignorant of the ecological, evolutionary and genetic processes that are inherent in maintaining natural populations. The new text by Frankham, Ballou and Briscoe could help to convince some that genetics does matter and that there is a need to preserve not only the pattern of biodiversity, but also the processes that produce and maintain it.The past three decades have seen the genesis and dramatic expansion of conservation genetics. Although journals now bulge at the seams with both empirical and theoretical papers, and several edited volumes have appeared detailing case studies and techniques, there has been no comprehensive textbook devoted exclusively to the field. Thus, An Introduction to Conservation Genetics fills an empty niche and should provide a nice foundation for courses in conservation genetics.My initial reaction was that the authors were trying a bit too hard to reach the naive reader, but after the introductory chapters the book finds its stride and does a good job covering topics from quantitative genetics to natural selection in small populations. One of the more notable attributes of the textbook is the attention the authors have given to the recent literature, with many of the examples and case studies taken from the last two years – a commendable feat for a book of over 600 pages.The book is subdivided into three sections. The first, comprising seven chapters, provides a thorough overview of the evolutionary genetics of natural populations. Although much of this material can be found in any introductory genetics text, the authors do a good job of providing case studies from a conservation perspective. For example, the fundamentals of genotype–environment interactions are first described, then they are discussed in the context of translocating individuals into new habitats. In a similar fashion, heritabilities are defined, followed by examples demonstrating how they are calculated in natural populations of various endangered species.The second section of the book is entirely devoted to the effects of small population size on genetic diversity and its causes. These five chapters emphasize the classic themes of conservation genetics – problems associated with small populations, inbreeding, habitat fragmentation and the challenges of retaining evolutionary potential within finite populations.The final section entitled ‘From Theory to Practice’ attempts to synthesize some of the major issues in conservation genetics. Rather than focusing on the more ubiquitous, but fundamentally flawed, evolutionary significant units (ESU) – an approach based solely on neutral genetic variation – I was pleased to see inclusion of a recent treatment of conservation units emphasizing the importance of adaptive variation [1xConsidering evolutionary processes in conservation biology: an alternative to ‘evolutionary significant units’. Crandall, K.A et al. Trends Ecol. Evol. 2000; 15: 290–295Abstract | Full Text | Full Text PDF | PubMed | Scopus (990)See all References[1].In the past, students interested in conservation genetics would need first to get the basics from the standard genetics texts, then to head to the primary literature. This new text book, intended for advanced undergraduates and graduate students, assumes a basic foundation in genetics and covers most, if not all, of the major topics in conservation genetics. Students will also appreciate several features of the book: important concepts are highlighted in a sentence or two at the edge of each page; boxes contain case studies or supplementary information to complement the text; and a concise summary section appears at the end of each chapter, along with problem sets (with answers in the back), suggested reading for the inspired and a comprehensive glossary. Some might quibble over the authors’ strong emphasis on some topics, such as small population size, but given its breadth and up-to-date treatment of the literature, the text should be of considerable value to students interested in conservation genetics and to the professional who needs a complete reference.

Species concepts versus species criteria: Response from Werner Kunz

Species concepts versus species criteria: Response from Werner Kunz

Ecology's oldest pattern?

Ecology's oldest pattern?

Mites on birds: Comment from Harper & Randall

Mites on birds: Comment from Harper & Randall

Do edge effects occur over large spatial scales?

In recent years, biologists have come to realize that one of the most important consequences of forest fragmentation is a dramatic increase in the amount of habitat edge 1 Janzen D.H. The eternal external threat. in: Soulé M.E. Conservation Biology: The Science of Scarcity and Diversity. Sinauer, 1986: 286-303 Google Scholar , 2 Lovejoy T.E. et al. Edge and other effects of isolation on Amazon forest fragments. in: Soulé M.E. Conservation Biology: The Science of Scarcity and Diversity. Sinauer, 1986: 257-285 Google Scholar . Although certain game species benefit from habitat ecotones, mounting evidence reveals that the abrupt, artificial edges created by forest fragmentation negatively affect many forest species and ecological processes 1 Janzen D.H. The eternal external threat. in: Soulé M.E. Conservation Biology: The Science of Scarcity and Diversity. Sinauer, 1986: 286-303 Google Scholar , 2 Lovejoy T.E. et al. Edge and other effects of isolation on Amazon forest fragments. in: Soulé M.E. Conservation Biology: The Science of Scarcity and Diversity. Sinauer, 1986: 257-285 Google Scholar , 3 Kapos V. Effects of isolation on the water status of forest patches in the Brazilian Amazon. J. Trop. Ecol. 1989; 5: 173-185 Crossref Scopus (446) Google Scholar , 4 Laurance W.F. et al. Biomass collapse in Amazonian forest fragments. Science. 1997; 278: 1117-1118 Crossref Scopus (467) Google Scholar , 5 Paton P.W.C. The effect of edge on avian nest success: how strong is the evidence?. Conserv. Biol. 1994; 8: 17-26 Crossref Scopus (668) Google Scholar , 6 Restrepo C. Gómez N. Responses of understory birds to anthropogenic edges in a neotropical montane forest. Ecol. Appl. 1998; 8: 170-183 Crossref Scopus (88) Google Scholar , 7 Laurance W.F. Bierregaard R.O. Tropical Forest Remnants: Ecology, Management, and Conservation of Fragmented Communities. University of Chicago Press, 1997 Google Scholar , 8 Didham R.K. An overview of invertebrate responses to habitat fragmentation. in: Watt A.D. Forests and Insects. Chapman & Hall, 1997: 303-320 Google Scholar , 9 Skole D. Tucker C. Tropical deforestation and habitat fragmentation in the Amazon: satellite data from 1978 to 1988. Science. 1993; 260: 1905-1910 Crossref PubMed Scopus (1157) Google Scholar , 10 Murcia C. Edge effects in fragmented forests: implications for conservation. Trends Ecol. Evol. 1995; 10: 58-62 Abstract Full Text PDF PubMed Scopus (2081) Google Scholar , 11 Laurance W.F. Edge effects in tropical forest fragments: application of a model for the design of nature reserves. Biol. Conserv. 1991; 57: 205-219 Crossref Scopus (274) Google Scholar . Edge effects and ecological processes: are they on the same scale?Ickes et al.Trends in Ecology & EvolutionSeptember 01, 2000In Brief Full-Text PDF

Conserved Ecological Niches

In their report “Conservatism of ecological niches in evolutionary time” (20 Aug., p. [1265][1]), A. T. Peterson et al. demonstrate that geographically isolated sister taxa show little differentiation in ecological niche. Their results imply that ecology diverges slowly in allopatry (the geographic isolation of species), and the authors therefore conclude that speciation most commonly occurs without significant ecological change. However, this conclusion seems to contradict the observation that sympatric sister taxa (species living in the same or overlapping locations) generally do show divergent ecology. Indeed, many sympatric ecological races are so closely related that hybridization still occurs regularly ([1][2]). We suggest two possible explanations for this discrepancy. First, as mentioned in the News of the Week article by Bernice Wuethrich (20 Aug., p. [1190][3]), the analysis considered only four physical factors in defining the niche of each species. Certainly, biotic factors such as feeding strategy, host plant use (in the case of butterflies), mutualisms, and predation are also important in defining the niche of a species. Thus, it may be that the analysis was simply too crude to show ecological divergence over a relatively short time scale. Alternatively, if Peterson et al. are correct and ecological divergence does in fact proceed rather slowly in allopatry, then we need another explanation for the frequent occurrence of sympatric, ecologically divergent sister taxa. Sympatric speciation, when it occurs, is likely to proceed rapidly because disruptive selection plays a direct role in driving divergence ([2][4]). In contrast, models of allopatric speciation do not generally invoke a direct role for natural selection and might thus be expected to proceed more slowly. By showing that allopatric divergence does not lead to rapid ecological change, Peterson et al. may have provided some of the best evidence that sympatric sister species have evolved in situ. 1. [↵][5]1. M. R. Orr, 2. T. B. Smith , Trends Ecol. Evol. 13, 502 (1998). [OpenUrl][6][CrossRef][7][PubMed][8][Web of Science][9] 2. [↵][10]1. U. Dieckmann, 2. M. Doebeli , Nature 400, 354 (1999). [OpenUrl][11][CrossRef][12][GeoRef][13] [1]: /lookup/doi/10.1126/science.285.5431.1265 [2]: #ref-1 [3]: /lookup/doi/10.1126/science.285.5431.1190a [4]: #ref-2 [5]: #xref-ref-1-1 View reference 1 in text [6]: {openurl}?query=rft.jtitle%253DTrends%2Bin%2BEcology%2B%2526%2BEvolution%26rft.stitle%253DTrends%2Bin%2BEcology%2B%2526%2BEvolution%26rft.aulast%253DOrr%26rft.auinit1%253DM.%2BR.%26rft.volume%253D13%26rft.issue%253D12%26rft.spage%253D502%26rft.epage%253D506%26rft.atitle%253DEcology%2Band%2Bspeciation.%26rft_id%253Dinfo%253Adoi%252F10.1016%252FS0169-5347%252898%252901511-0%26rft_id%253Dinfo%253Apmid%252F21238408%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [7]: /lookup/external-ref?access_num=10.1016/S0169-5347(98)01511-0&link_type=DOI [8]: /lookup/external-ref?access_num=21238408&link_type=MED&atom=%2Fsci%2F286%2F5438%2F239.5.atom [9]: /lookup/external-ref?access_num=000077403800010&link_type=ISI [10]: #xref-ref-2-1 View reference 2 in text [11]: {openurl}?query=rft.jtitle%253DNature%253B%2BPhysical%2BScience%2B%2528London%2529%26rft.stitle%253DNature%253B%2BPhysical%2BScience%2B%2528London%2529%26rft.volume%253D400%26rft.issue%253D6742%26rft.spage%253D354%26rft.epage%253D357%26rft.atitle%253DOn%2Bthe%2Borigin%2Bof%2Bspecies%2Bby%2Bsympatric%2Bspeciation%26rft_id%253Dinfo%253Adoi%252F10.1038%252F22521%26rft.genre%253Darticle%26rft_val_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Ajournal%26ctx_ver%253DZ39.88-2004%26url_ver%253DZ39.88-2004%26url_ctx_fmt%253Dinfo%253Aofi%252Ffmt%253Akev%253Amtx%253Actx [12]: /lookup/external-ref?access_num=10.1038/22521&link_type=DOI [13]: /lookup/external-ref?access_num=1999055575&link_type=GEOREF

RNAs from all categories generate retrosequences that may be exapted as novel genes or regulatory elements.

While the significance of middle repetitive elements had been neglected for a long time, there are again tendencies to ascribe most members of a given middle repetitive sequence family a functional role--as if the discussion of SINE (short interspersed repetitive elements) function only can occupy extreme positions. In this article, I argue that differences between the various classes of retrosequences concern mainly their copy numbers. Consequently, the function of SINEs should be viewed as pragmatic such as, for example, mRNA-derived retrosequences, without underestimating the impact of retroposition for generation of novel protein coding genes or parts thereof (exon shuffling by retroposition) and in particular of SINEs (and retroelements) in modulating genes and their expression. Rapid genomic change by accumulating retrosequences may even facilitate speciation [McDonald, J.F., 1995. Transposable elements: possible catalysts of organismic evolution. Trends Ecol. Evol. 10, 123-126.] In addition to providing mobile regulatory elements, small RNA-derived retrosequences including SINEs can, in analogy to mRNA-derived retrosequences, also give rise to novel small RNA genes. Perhaps not representative for all SINE/master gene relationships, we gained significant knowledge by studying the small neuronal non-messenger RNAs, namely BC1 RNA in rodents and BC200 RNA in primates. BC1 is the first identified master gene generating a subclass of ID repetitive elements, and BC200 is the only known Alu element (monomeric) that was exapted as a novel small RNA encoding gene.

Congruence Between Phylogeny and Stratigraphy: Randomization Tests and the Gap Excess Ratio

Stratigraphic congruence indices (e.g., stratigraphic consistency index [SCI] of Huelsenbeck, 1994, Paleobiology 40:563–569; relative completeness index [RCI] of Benton, 1994, Trends Ecol. Evol. 9:181–185 [not to be confused with the rescaled consistency index of Farris, 1989, Cladistics 5:417–419]) are increasingly being quoted for cladograms containing fossil taxa. However, like the character consistency index (CI, summed over all characters), these values cannot be compared for trees derived from different data sets. Just as the number of characters and taxa in data matrices affects typical CI values, so tree balance and the distribution of stratigraphic ranges (and indirectly tree size) delimit the range of congruence indices that can be obtained. Because investigators often seek to compare the performance of cladograms from different sources (e.g., different taxa, habitats, periods in history), indices of fit insensitive to these factors are desirable. Two approaches are proposed here: (1) The gap excess ratio (GER) is a new metric that controls for the distribution of range data but is sensitive to differences in tree balance. The GER expresses the difference between the minimum implied gap (MIG; the total ghost range implied by a given set of stratigraphic ranges on a given tree) and Gmin (the minimum possible ghost range for those data on any tree) as a fraction of the range of values possible for those stratigraphic data on any tree. Rather than reflecting inferred completeness of the fossil record (as does the RCI, which is only partially determined by cladistic constraints), the GER indicates congruence alone. (2) Randomization tests hold most potentially conflated parameters constant and compare the observed RCI or GER index with the distribution of indices obtained by randomly reassigning range data over the tree. This enables us to deduce whether the MIG is significantly less (i.e., shows greater congruence) than for random permutations of the same range data. Stratigraphic congruence indices have been invoked as an ancillary criterion for assessing competing hypotheses of relationships derived from different sources or for choosing between equally parsimonous trees derived from the same character matrix. The first application is illustrated with comparisons of actinopterygian and eutherian phylogenies, and the second is illustrated with a study of trees for fossil and Recent arthropods.

Deep flowers for long tongues: reply from L.A. Nilsson

The core for disagreement about the tongue-flower elongation, coevolution versus non-coevolution, is whether a long hawkmoth tongue is used primarily for feeding or for predator avoidance. Wasserthal[1xWasserthal, L.T. Trends Ecol. Evol. 1998; 13: 459–460Abstract | Full Text | Full Text PDF | PubMedSee all References][1]considers his predation hypothesis for tongue length confirmed, but his three cited papers lack quantitative data on natural predation. Svensson et al.[2xSvensson, M.G.E., Rydell, J., and Tove, J. Trends Ecol. Evol. 1998; 13: 460Abstract | Full Text | Full Text PDF | PubMedSee all References][2]argue in support of his interpretation by anecdotal evidence. They miss the flight–elongation focus. However, I agree with them and with Samways[3xSamways, M.J. Trends Ecol. Evol. 1998; 13: 460Abstract | Full Text | Full Text PDF | PubMedSee all References][3]that major predation on large hawkmoths is expected from flying vertebrates, not arthropods in ambush a la Wasserthal.Nectar-extracting mouthparts have attained impressive extremes in euglossine bees (4 cm), nemestrinid flies (8 cm) and hummingbirds (10 cm), each set of taxa using/pollinating a unique guild of deep-flowered plants[4xSchremmer, F. Verh. D. Zool. Ges. (Suppl.). 1961; 25: 375–401See all References, 5xSee all References]. Nothing suggests that predator avoidance has influenced the elongation (co)evolution. Long-tongued hawkmoths and their deep flowers, although displaying world records (30 cm and 40 cm, respectively), are hardly exceptions in this respect. The various very deep-flowered angiosperms (e.g. Epiphyllum in neotropical Cactaceae) are probably coevolved with hawkmoth tongues.Hawkmoth flight repertoires include `on-the-spot' hovering as well as `swing-hovering' during flower-visits. Also, hummingbirds, long-tongued solitary bees (euglossines, anthophorids) and long-tongued flies (horseflies, nemestrinid and bee flies) hover on-the-spot. No doubt this behaviour favours targeting and insertion precision with the extended mouthparts into narrow nectariferous structures. Extremely long-tongued hawkmoths probably require even more precision control. Added swing-hovering may increase visual and/or olfactory information about the position of the flower. Anti-predator adaptations, on the other hand, are to be expected among other traits.Basal hawkmoth clades contain the long-tongued taxa[6xRothschild, L.W. and Jordan, K. Nov. Zool. 1903; 9: 1–972See all References][6]. But modern phylogenetic analyses (so badly needed!) are likely to show a very long tongue to be a derived, relatively late trait within several lines (e.g. Amphimoea, Coelonia). Furthermore, very long-tongued hawkmoths might not be true generalists but instead might have have guild constancy under natural, undisturbed conditions. Their opportunistic exploitation of pantropical weedy Lantana[7xWasserthal, L.T. Bot. Acta. 1997; 110: 1–17CrossRefSee all References][7], a lepidopteran-adapted species, is hardly surprising.Wasserthal's argument that `obligate synchrony and syntopy' of Xanthopan morganii praedicta and Angraecum sesquipedale would have been required for coevolution is flawed. These interactors are participants of coevolving guilds[8xNilsson, L.A. et al. Biotropica. 1987; 19: 310–318CrossRefSee all References][8]. Various pollinator shifts may well have occurred, as are commonplace in the history of orchids and other angiosperms[9xVogel, S. Bot. Stud. 1954; 1: 1–338See all References, 10xJohnson, S.D., Linder, H.P., and Steiner, K.E. Am. J. Bot. 1997; 85: 402–411CrossRefSee all References]. Coevolution and shifting occur by relatively `better' pollinators. The basis for Darwin's reciprocal-effect model is that a competitive visitor with a non-bottom-reaching tongue better contacts the flower's pollination organs[11xSee all References][11]. The depth of spur and the length of reward-extracting organ become inter-dependent and matching at the population level[12xSteiner, K.E. and Whitehead, V.B. Evolution. 1990; 44: 1701–1707CrossRefSee all References][12]. A consistently bottom-reaching, although competitive, hawkmoth tongue excludes pollinator shifts, as indicated by Xanthopan on Angraecum compactum[7xWasserthal, L.T. Bot. Acta. 1997; 110: 1–17CrossRefSee all References][7]. Some 100 Madagascan angraecoids have demonstrably retained adaptation to medium-tongued hawkmoths. Angraecum sesquipedale, guild-member angiosperms, Xanthopan and major hawkmoth competitors are evidently coevolved.The intention of Wasserthal's study has not been overlooked, nor has the difficulty of obtaining natural interaction data. Our team still recorded frequent pollination of A. sesquipedale in 1983 and 1986. Wasserthal's study of the same populations, species and systems in Madagascar has partly led to more questions than answers, and he has yet to adopt a plausible evolutionary interpretation of his observations.

Trace fossils and the Cambrian explosion

In two recent contributions to TREE[1xThomas, A.R.L. Trends Ecol. Evol. 1998; 13: 129Abstract | Full Text | Full Text PDF | PubMedSee all References, 2xThomas, A.R.L. Trends Ecol. Evol. 1998; 13: 322Abstract | Full Text | Full Text PDF | PubMedSee all References], Thomas has argued that trace fossils (trails, burrows, etc.) support deep Precambrian divergence of metazoans, and concludes that the Cambrian explosion is a taphonomic event of the appearance of hard parts. Speaking from experience, he calls upon `Ediacaran' sites in Sweden said to have beautifully preserved the Precambrian sea floor with an `astonishing abundance of trace fossils'. This would be indeed compelling evidence—except that there are no Ediacaran sites in Sweden. Reference to the occurrence of Psammocorallia, however, shows that Thomas is thinking of the Mickwitzia sandstone[3xJensen, S. Fossils & Strata. 1997; 42: 1–110See all References[3]. This unit is actually late Early Cambrian. In fact, there are no convincing trace fossils anywhere in the world older than 600 Ma (Ref. [4xSee all References[4]) and all moderately diverse terminal Proterozoic trace fossil assemblages may be younger than 550 Ma (Ref. [5xGrotzinger, J.P. et al. Science. 1995; 270: 598–604CrossrefSee all References[5]).Trace fossils do not suffer from the same taphonomic peculiarities that complicate arguments about the nature of the soft-bodied Ediacara-type fossils. Unless contrived ad hoc hypotheses are to be invoked, it may thus be safely assumed that their appearance marks the appearance of macroscopic bilaterians.Additionally we would like to comment on the frequently-aired hypothesis of cryptic evolution of miniature Precambrian metazoans[6xFortey, R.A., Briggs, D.E.K., and Wills, M.A. BioEssays. 1997; 19: 429–434CrossrefSee all References, 7xCooper, A. and Fortey, R. Trends Ecol. Evol. 1998; 13: 151–156Abstract | Full Text | Full Text PDF | PubMed | Scopus (119)See all References]. In this scheme the Cambrian explosion is seen as little more than an increase in size and, in some groups, the acquisition of hard parts, in already well-separated lineages. However, such miniature stem-group animals would have faced extremely different ecological conditions to macroscopic animals, and it is difficult to see how many of the shared morphological features of the modern phyla—such as blood vascular systems[8xRuppert, E.E. and Carle, K.J. Zoomorphology. 1983; 103: 193–208Crossref | Scopus (54)See all References[8]and body cavities—could have been functionally useful in such a setting. Either these features were acquired in an avalanche of convergence in the separate lineages, or—much more likely—characters that are used to define eumetazoan phyla appeared in the latest Vendian–Cambrian and in most cases even later. This in turn would imply that the cladogenesis leading to the modern phyla is indeed accurately reflected by the increase in diversity of trace and body fossils from the latest Vendian to the Cambrian, a gradual process taking at least 20 million years. We conclude that `accurate' analysis of the fossil evidence strongly suggests the Cambrian explosion is a reality representing the origins of first stem-group and then crown-group members of the Bilateria.

Reply from S. Randolph

Kelly's work offers hope that the full distribution of seed crops produced by a number of tree species, from crop failure to so-called `masting' events[1xKelly, D. Trends Ecol. Evol. 1994; 13: 301–303See all References[1], may be predictable from weather patterns. It does not, however, strengthen Jones et al.'s[2xJones, C.G. et al. Science. 1998; 279: 1023–1026Crossref | PubMed | Scopus (255)See all References[2]speculative link between the size of acorn crops and the prevalence of spirochaetes (Borrelia burgdorferi) that cause Lyme disease, which remains untested and unproven. There is little doubt that the white-footed mouse, Peromyscus leucopus, plays an important role in B. burgdorferi transmission in the eastern USA, but Jones' own data raise the possibility that other host species are feeding significant numbers of immature ticks.Mather[3xSee all References[3]considered only variable mouse densities, not changing numbers of larval ticks nor of any other host species such as deer or chipmunks. Whether or not these hosts contribute to spirochaete transmission, the effect that they may have on spirochaete prevalence in the nymphal tick population two years after an unusually large acorn crop remains to be investigated before masting may be used as a reliable predictor of future Lyme disease risk.

Mast seeding and Lyme disease

We wish to comment on two issues relating to a prediction raised in the article by Randolph[1xRandolph, S.E. Trends Ecol. Evol. 1998; 13: 301–303Abstract | Full Text | Full Text PDF | PubMed | Scopus (7)See all References[1]about our work[2xJones, C.G. et al. Science. 1998; 279: 1023–1026Crossref | PubMed | Scopus (255)See all References[2]. Randolph argues that because `low acorn production and moderate mouse densities are the norm [our] data do not explain the cause of the severe acorn failures and contingent crash in mouse populations that might initiate [gypsy] moth outbreaks'. We made no attempt to explain masting periodicity, but autumnal mast production does predict white-footed mouse (Peromyscus leucopus) density the following summer[3xWolff, J.O. J. Mammol. 1996; 77: 850–856CrossrefSee all References, 4xOstfeld, R.S., Jones, C.G., and Wolff, J.O. Bioscience. 1996; 46: 323–330CrossrefSee all References, 5xElkinton, J.S. et al. Ecology. 1996; 77: 2332–2342CrossrefSee all References]. Moderate mouse densities are indeed the norm. In most summers, densities are at or above c. 10 mice ha−1, which is sufficient to keep gypsy moth (Lymantria dispar) populations low via pupal predation[4xOstfeld, R.S., Jones, C.G., and Wolff, J.O. Bioscience. 1996; 46: 323–330CrossrefSee all References, 5xElkinton, J.S. et al. Ecology. 1996; 77: 2332–2342CrossrefSee all References, 6xElkinton, J.S. and Liebhold, A.M. Annu. Rev. Entomol. 1990; 35: 571–596CrossrefSee all References]. However, mouse populations do periodically collapse to below 10 ha−1 for one to two summers[3xWolff, J.O. J. Mammol. 1996; 77: 850–856CrossrefSee all References, 4xOstfeld, R.S., Jones, C.G., and Wolff, J.O. Bioscience. 1996; 46: 323–330CrossrefSee all References]. Evidence indicates that this is when moth populations, with their high fecundity, can rise to levels mice cannot suppress[2xJones, C.G. et al. Science. 1998; 279: 1023–1026Crossref | PubMed | Scopus (255)See all References, 4xOstfeld, R.S., Jones, C.G., and Wolff, J.O. Bioscience. 1996; 46: 323–330CrossrefSee all References, 5xElkinton, J.S. et al. Ecology. 1996; 77: 2332–2342CrossrefSee all References]. Mouse population collapses tend to occur if major masting events, which result in very high mouse densities, are followed by mast failure and food limitation. These events occur with a frequency similar to moth outbreaks[3xWolff, J.O. J. Mammol. 1996; 77: 850–856CrossrefSee all References, 4xOstfeld, R.S., Jones, C.G., and Wolff, J.O. Bioscience. 1996; 46: 323–330CrossrefSee all References].Randolph challenges our conclusion that white-footed mice play the major role in infecting Ixodes scapularis ticks with Borrelia burgdorferi. However, in the eastern United States, P. leucopus is both the most abundant host for ticks and by far the most competent reservoir for B. burgdorferi[7xSee all References[7]. Furthermore, Mather and Ginsberg[8xSee all References[8]demonstrated that the prevalence of spirochete infection in nymphal I. scapularis ticks strongly correlates with white-footed mouse density in the previous year. In our forests, acorns markedly affect mouse density, the density of host-seeking larval ticks and the number of ticks attached to mice[2xJones, C.G. et al. Science. 1998; 279: 1023–1026Crossref | PubMed | Scopus (255)See all References[2]. Therefore, we conclude that acorn production should allow epidemiologists to predict Lyme disease risk well in advance, here in the USA[9xOstfeld, R.S. Am. Sci. 1997; 85: 338–346See all References[9]. The European situation, in which several tick hosts are competent reservoirs, will probably make predicting Lyme disease risk more difficult. Nevertheless, we hope that epidemiologists will test the power of acorn production as a predictor of Lyme disease risk in European oak forests.

Reply from T.H. Clutton-Brock

I welcome Emlen, Reeve and Keller's recognition that it is difficult to distinguish between cases where subordinates reproduce because dominants are unable to prevent them from doing so and cases where dominants allow subordinates a share of reproduction to induce them to remain in the group and assist in future breeding attempts [as optimal skew models (OSMs) suggest]. I am also in full agreement with them that the presence of overt conflict does not contradict the predictions of OSMs, since dominants might use the responses of subordinates to assess the magnitude of incentives necessary to retain their services. Indeed, as I make this point on page 289 of my review[1xClutton-Brock, T.H. Trends Ecol. Evol. 1998; 13: 288–292Abstract | Full Text | Full Text PDF | PubMed | Scopus (209)See all References[1], I am uncertain whose misunderstandings it is important to correct.However, I believe that the burden of evidence is on those wishing to interpret subordinate breeding as the outcome of reproductive contracts between dominants and subordinates to show that it is not merely the result of a failure of control. This is partly because there is plenty of evidence that dominant animals do not exert full control over subordinate reproduction in societies where subordinates do not assist (and OSMs do not apply). In addition, OSMs rely on a range of untested assumptions, including the assumptions that subordinates that are allowed to breed are less likely to challenge the dominant and that the benefits of retaining a subordinate (to the dominant) exceed the costs of allowing them to breed[1xClutton-Brock, T.H. Trends Ecol. Evol. 1998; 13: 288–292Abstract | Full Text | Full Text PDF | PubMed | Scopus (209)See all References[1].I am also sceptical that testing predictions about the distribution of reproduction will ever provide unambiguous evidence of the kind of social contract envisaged by concession models. Many of the same social and environmental variables are likely to affect both the costs and benefits of attempting to breed (to subordinates) and the benefits of granting reproductive benefits (to dominants) so that firm, contrasting predictions are uncommon. Moreover, the OSMs and incomplete control models (ICMs) published by Emlen and his co-workers represent a small fraction of the range of credible models that could be built to predict skew[2xCant, M.A. Anim. Behav. 1998; 55: 163–169Crossref | PubMed | Scopus (101)See all References, 3xSee all References], so that it is usually possible to suggest reasonable modifications to OSMs and ICMs that are likely to affect their predictions. The most convincing evidence of reproductive contracts of the kind envisaged by OSMs will come from studies that manipulate the benefits of retaining subordinates to individual dominants and show that this affects their tolerance of breeding subordinates. Only direct evidence of changes in the behaviour of dominants is, I believe, likely to show unequivocally whether reproductive contracts occur. My own guess is that, among vertebrates, reproductive contracts will prove to be rare among females but more common between cooperating males[1xClutton-Brock, T.H. Trends Ecol. Evol. 1998; 13: 288–292Abstract | Full Text | Full Text PDF | PubMed | Scopus (209)See all References[1].

Deep flowers for long tongues

Nilsson[1xNilsson, L.A. Trends Ecol. Evol. 1998; 13: 259–260Abstract | Full Text | Full Text PDF | PubMed | Scopus (50)See all References][1]presents a cogent argument in support of Darwin's classic model of a coevolutionary relationship between long moth-tongues and deep corollas. This is no mean feat on the part of the moth. Convolvulus hawks (Herse convolvuli) in South Africa insert their 10 cm tongues within a fraction of a second, hover for less than 3 seconds and then move to the next flower. The tongues are indeed inserted so that the head is close to the corolla opening. It is done with such accuracy and speed that strong selection pressures are presumably at work. Several hundred flowers from various individual plants are visited in one night. A dozen or so moths may be in the local area for two or three nights and then all the moths move on to a new site.Can we exclude predation as a selective force in this behaviour? Might current behaviour be a ghost of past selection pressures? Convolvulus hawkmoths hover steadily; there is no side-to-side movement—indeed, they appear almost fixed. A solid-substrate based predator like a mantid or spider would have to find purchase in order to strike, and it would not have a firm foothold on a flimsy corolla. Much more likely is predation from flying predators—bats. But can such a predator approach the feeding prey unhindered? On balance, Nilsson[1xNilsson, L.A. Trends Ecol. Evol. 1998; 13: 259–260Abstract | Full Text | Full Text PDF | PubMed | Scopus (50)See all References][1]is probably correct in that the primary driver has been coevolution between plant and moth, but if it were not for flying predators, the interaction might not have the exquisite elegance we see today.

Deep flowers for long tongues

Darwin[ 1 Darwin, C. (1862) On the Various Contrivances by which British and Foreign Orchids are Fertilized by Insects, John Murray Google Scholar ]explained deep-spurred flowers as adaptations to long-tongued pollinators. This spur elongation model was experimentally tested in some European orchids with rather short spurs[ 2 Nilsson L.A. Nature. 1988; 334: 147-149 Crossref Scopus (405) Google Scholar ]. The reciprocal effect in the coevolutionary race model[ 1 Darwin, C. (1862) On the Various Contrivances by which British and Foreign Orchids are Fertilized by Insects, John Murray Google Scholar ], postulating that the long tongues evolved as adaptation to exploit long-tubed flowers—favoured in Nilsson's news & comment article[ 3 Nilsson L.A. Trends Ecol. Evol. 1998; 13: 259-260 Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar ]about my paper[ 4 Wasserthal L.T. Bot. Acta. 1997; 110: 1-17 Crossref Scopus (110) Google Scholar ]—has never been confirmed. The pollinator shift model[ 4 Wasserthal L.T. Bot. Acta. 1997; 110: 1-17 Crossref Scopus (110) Google Scholar ]is a modification of the spur elongation model, entailing the `driving force' of a nectar-exploiting competitor with a longer tongue than the `legitimate' pollinator(s). It was established after the following facts and arguments favouring the hypothesis that long tongues evolved for predator avoidance[ 5 Wasserthal, L.T. (1993) in Animal–Plant Interactions in Tropical Environments (Barthlott, W. et al., eds), pp. 77–87, Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn Google Scholar , 6 Wasserthal L.T. Zoology. 1998; 101: 34 Google Scholar , 7 Wasserthal, L.T. (1996) German Research Rept. DFG 1/96, 22–25 Google Scholar ]: •Individuals of European long-tongued hawkmoths (Agrius convolvuli) exhibited a swing-hovering behaviour and were incapable of inserting their tongues into long-tubed tobacco flowers[ 5 Wasserthal, L.T. (1993) in Animal–Plant Interactions in Tropical Environments (Barthlott, W. et al., eds), pp. 77–87, Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn Google Scholar ]. •Swing-hovering has been discovered in almost all long-tongued Malagasy hawkmoths and recently in several related Central/South American species[ 5 Wasserthal, L.T. (1993) in Animal–Plant Interactions in Tropical Environments (Barthlott, W. et al., eds), pp. 77–87, Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn Google Scholar , 6 Wasserthal L.T. Zoology. 1998; 101: 34 Google Scholar ]. •In primarily nonswinging individuals, swing-hovering could be induced by simulated predator stimuli[ 5 Wasserthal, L.T. (1993) in Animal–Plant Interactions in Tropical Environments (Barthlott, W. et al., eds), pp. 77–87, Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn Google Scholar ]and ctenid spiders in Costa Rica. •Heteropodid spiders in Madagascar systematically pursue and jump at shivering or hovering moths[ 7 Wasserthal, L.T. (1996) German Research Rept. DFG 1/96, 22–25 Google Scholar ]. •Long-tongued hawkmoths are generalist feeders; they skilfully exploit small and shallow flowers (e.g. of Verbenaceae[ 5 Wasserthal, L.T. (1993) in Animal–Plant Interactions in Tropical Environments (Barthlott, W. et al., eds), pp. 77–87, Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn Google Scholar ]). •The Old World Xanthopan and the New World Cocytius are regarded as close relatives, with their very long tongue being a basic trait of ancestral Sphingicae and Acherontiicae[ 8 Rothschild L.W. Jordan K. Novit. Zool. 1903; 9: 1-972 Google Scholar ]. •Their hairy caterpillars feed on primitive angiosperms (Annonaceae)[ 7 Wasserthal, L.T. (1996) German Research Rept. DFG 1/96, 22–25 Google Scholar , 9 Moss A.M. Novit. Zool. 1920; 27: 334-415 Google Scholar ]. •The sphingophilous long-tubed flowers, especially the orchids, are of more recent origin, and the ancestors of their modern pollinators visited less-specialized flowers of older plant families[ 10 van der Pijl, L. and Dodson, C.H. (1966) Orchid Flowers, their Pollination and Evolution, University of Miami Press Google Scholar ].

Quantifying brain–behavior relations in cetaceans and primates

In their recent TREE review, Connor et al.[1xConnor, R.C. et al. Trends Ecol. Evol. 1998; 13: 228–232Abstract | Full Text | Full Text PDF | PubMed | Scopus (116)See all References][1]provide an excellent and thought-provoking comparison of behavioral ecological patterns between toothed whales (odontocetes) and terrestrial mammals, particularly primates. The authors end their review with a provocative call for efforts to quantify the relationship between behavioral ecology and brain size among odontocetes in a similar manner to Dunbar's analyses for primates[2xDunbar, R.I.M. J. Hum. Evol. 1992; 20: 469–493CrossRef | Scopus (618)See all References, 3xDunbar, R.I.M. Evol. Anthropol. 1998; 6: 178–190CrossRefSee all References]. Nevertheless, in doing so they leave the reader with the impression that these quantitative studies have not yet been attempted. There are two studies that do exemplify the very approach Connor et al. advocate. These studies provide quantitative support for the `combination of convergence and novelty'[1xConnor, R.C. et al. Trends Ecol. Evol. 1998; 13: 228–232Abstract | Full Text | Full Text PDF | PubMed | Scopus (116)See all References][1]suggested by observational and qualitative comparisons of brain and behavior between odontocetes and primates.First, there is a significant positive correlation between pod size and encephalization quotient (a measure of relative brain size taking into account brain–body allometry) among 21 odontocete species from all six odontocete families[4xMarino, L. Evol. Anthropol. 1996; 5: 81–85CrossRefSee all References][4]. Therefore, the relationship between one measure of sociality (i.e. social group size and brain size) appears to be similar in primates and odontocetes.Second, although there is a positive correlation between encephalization level and gestation length among primates[5xSee all References][5], in an analysis using the same encephalization values for the 21 odontocete species already mentioned, there is no significant relationship between encephalization and gestation length among odontocetes[6xMarino, L. Mar. Mamm. Sci. 1997; 13: 133–138CrossRefSee all References][6]. Rather, body size accounts for more of the variation in gestation length than encephalization among odontocetes. Therefore, there is quantitative evidence for differences in brain and life history relationships across primates and odontocetes.My point here is not to criticize Connor et al. but to strengthen and extend their emphasis on quantitative analyses of odontocete behavioral ecology by showing that these kinds of studies are already underway. It is, of course, important to continue to further these studies while moving towards formulating and testing hypotheses about the evolution of cetacean brain–behavioral relationships and its implications for general mammalian evolution.

On hotspots and the use of indicators for reserve selection

In a wide-ranging and stimulating TREE review, Reid[1xReid, W.V. Trends Ecol. Evol. 1998; 13: 275–280Abstract | Full Text | Full Text PDF | PubMed | Scopus (305)See all References[1]recently concluded that focusing on a handful of readily surveyed indicator groups could be of limited use in identifying priorities for conserving biodiversity as a whole. His reason was straightforward: a suite of studies[2xPrendergast, J.R. et al. Nature. 1993; 365: 335–337CrossrefSee all References, 3xLombard, A.T. S. Afr. J. Zool. 1995; 30: 145–163See all References, 4xDobson, A.P. et al. Science. 1997; 275: 550–553Crossref | PubMed | Scopus (396)See all References, 5xFlather, C.H. et al. Ecol. Appl. 1997; 7: 531–542CrossrefSee all References]has now shown that, at the relatively fine scales relevant to reserve planning, there is often little correspondence in the richest sites for different groups (see also Refs [6xGaston, K.J. Prog. Phys. Geogr. 1996; 20: 105–112CrossrefSee all References[6]and [7xvan Jaarsveld, A.S. et al. Science. 1998; 279: 2106–2108Crossref | PubMed | Scopus (242)See all References[7]). Hotspots—defined variously as the richest sites for all species, or for endemic, rare or threatened species—seldom coincide across taxa.More importantly (and not explicitly discussed by Reid), other studies[4xDobson, A.P. et al. Science. 1997; 275: 550–553Crossref | PubMed | Scopus (396)See all References, 7xvan Jaarsveld, A.S. et al. Science. 1998; 279: 2106–2108Crossref | PubMed | Scopus (242)See all References]show that sets of priority sites identified by considering between-site complementarity, as well as species richness (which therefore represent diversity far more efficiently than do hotspots[8xPressey, R.L. et al. Trends Ecol. Evol. 1993; 8: 121–128Abstract | Full Text PDF | Scopus (655)See all References, 9xWilliams, P.H. et al. Conserv. Biol. 1996; 10: 155–174CrossrefSee all References]), also show poor cross-taxon overlap. However, although high congruence in the most important sites for conserving different kinds of organisms would be extremely useful for conservation planning (and fascinating from an evolutionary perspective), its absence is not sufficient justification for rejecting the use of indicators for reserve selection. This is because whether the priority sites for one group embrace priority areas for other taxa is fundamentally less important than the extent to which they capture species from those taxa.What really matters in testing the use of indicators for reserve selection is the representation of diversity as a whole in the key sites for just one focal group. Towards the end of his review, Reid mentions unpublished results from Oregon (referred to in Ref. [10xCsuti, B. et al. Biol. Conserv. 1997; 80: 83–97Crossref | Scopus (298)See all References[10]) showing that cross-taxon capture of species by the complementary sites for single taxa is actually rather high. Another recent review cites similar evidence from other studies[5xFlather, C.H. et al. Ecol. Appl. 1997; 7: 531–542CrossrefSee all References[5]. An extensive new analysis across 50 forest reserves in Uganda confirms these findings and provides an explanation for them, which in turn suggests that, in some areas, the use of indicators for reserve selection holds more promise than Reid seems to imply[11xSee all References[11].Working on a dataset covering 2452 species of woody plants, large moths, butterflies, birds and small mammals that took nearly 100 man-years of survey effort to compile, Howard and colleagues[11xSee all References[11]first showed that in Uganda, as elsewhere, patterns of species richness (controlling for forest area) show poor congruence across groups. Nevertheless, complementarity-based sets of priority sites identified using data on single taxa capture species richness across all groups with roughly the same efficiency as sets built up using information on all taxa; data on birds and butterflies perform particularly well. The reason is that Uganda is environmentally quite heterogeneous, and each taxon exhibits similar biogeographical patterns across the country. Consequently, pairs of forests that complement each other well for one taxon do so for other groups too, and a priority set for one taxon embraces all the main habitat types for other groups. In this case, lack of cross-taxon congruence in species richness is not enough to invalidate the use of indicators because of high congruence in complementarity.How general are these results likely to be? Other studies have shown that complementary areas for focal taxa sometimes capture diversity in other groups rather less well than in Uganda, but these deal with temperate situations where the focal taxa themselves are relatively species-poor[12xRyti, R.T. Ecol. Appl. 1992; 2: 404–410CrossrefSee all References[12], or contain far fewer species than there are candidate sites for their conservation[4xDobson, A.P. et al. Science. 1997; 275: 550–553Crossref | PubMed | Scopus (396)See all References[4]. Further work is now needed to assess whether the Uganda results hold for less heterogeneous parts of the tropics, where high species richness coupled with very limited funds for biodiversity surveys suggest that the payoffs of using indicators for reserve selection would be greatest.

The role of soil community in plant population dynamics: is allelopathy a key component?

In his recent TREE news & comment, Watkinson[ 1 Watkinson A.R. Trends Ecol. Evol. 1998; 13: 171-172 Abstract Full Text PDF PubMed Google Scholar ]drew attention to the role of soil microorganisms in plant population dynamics. In particular, he reported on the dynamical framework for the inter-relations between the composition of plant and soil communities, proposed last year by Bever et al.[ 2 Bever J.D. Westover K.M. Antonovics J. J. Ecol. 1997; 85: 561-573 Crossref Scopus (771) Google Scholar ]It is worth adding allelopathic interactions to this picture.

Reply from J.L. Bossart and D. Pashley Prowell

We thank Bohonak et al. for the opportunity to expand upon our perspective of gene flow estimates[1xBossart, J.L. and Prowell, D.P. Trends Ecol. Evol. 1998; 13: 202–206Abstract | Full Text PDF | PubMed | Scopus (375)See all References][1]. We are comfortable with our portrayal of the state of this field based on data from Evolution. Evolution was selected because it has a long history as a top journal focusing on empirically based population genetics, has a vast readership and high citation rates. Molecular Ecology, however, is a new, more specialized and less available journal.We agree that most indirect studies of gene flow report data for multiple loci and many use resampling techniques or regression to conduct sensitivity analyses. The issue is whether these are informative comparisons. For example, have estimates averaged over loci advanced our understanding of gene frequency evolution when estimates among loci vary, not uncommonly, by orders of magnitude[2xTempleton, A.R. Mol. Ecol. 1998; 7: 381–398CrossRef | PubMed | Scopus (898)See all References][2]?Our perspective acknowledged problems associated with direct measures of dispersal. Like others[3xSlatkin, M. Annu. Rev. Ecol. Syst. 1985; 16: 393–430CrossRefSee all References][3], however, we emphasized the essential information these estimates provide. Correlational approaches between Fst and life history traits to assess accuracy of genetic methods, as advocated by Bohonak et al., are statistically weak and confounded by evolutionary history—for example, higher Fst values in sessile versus vagile organisms may reflect vicariant events.Application of conventional indirect methods to address ecological questions is inappropriate for two reasons. First, there is no temporal reference point. Do data reveal processes operating over ten years, 100 years, 1000 years or 10 000 years? Second, Nm changes only trivially between Nm=2 and Nm=infinity, so Nm=2 is virtually indistinguishable from Nm=2000 (Ref. [2xTempleton, A.R. Mol. Ecol. 1998; 7: 381–398CrossRef | PubMed | Scopus (898)See all References][2]). Thus, conventional approaches have insufficient power to address relative rates of gene flow among populations impinged upon by human activities, metapopulation dynamics, trophic interactions or relative magnitude of gene flow versus selection.Our overall conclusion that indirect methods `provide a useful starting point'[1xBossart, J.L. and Prowell, D.P. Trends Ecol. Evol. 1998; 13: 202–206Abstract | Full Text PDF | PubMed | Scopus (375)See all References][1]was mirrored by Bohonak et al. in their statement that indirect methods `provide a valuable first approximation'. We part company, however, on the widespread use of new analytical models, as our review validated. As this changes, the field will advance.

Reply from N.E. Langmore

Although female song for mate attraction could well be more widespread than is currently thought, the examples presented by Eens and Pinxten highlight the difficulties of inferring function in the absence of detailed, experimental studies. For example, in the experimental study they refer to, two out of nine female blue tits sang after their mates had been removed, suggesting that they were singing to attract a new mate. However, three of these nine females were also reported to engage in fights with neighbouring females[1xKempenaers, B. et al. Behav. Ecol. Sociobiol. 1995; 36: 33–42Crossref | Scopus (105)See all References[1]. As blue tits are facultatively polygynous[1xKempenaers, B. et al. Behav. Ecol. Sociobiol. 1995; 36: 33–42Crossref | Scopus (105)See all References[1], it is equally plausible that female song in this species could function in female–female aggression, as has been observed in many other facultatively polygynous species[2xLangmore, N.E. Trends Ecol. Evol. 1998; 13: 136–140Abstract | Full Text | Full Text PDF | PubMed | Scopus (155)See all References[2], rather than for mate attraction. It would be interesting to know if the female songs described in the other studies were also associated with female–female aggression. Although the possibility that females sing to attract extra-pair males is intuitively appealing, an experimental study of female song in the species with the highest incidence of extra-pair paternity failed to find any support for this hypothesis[3xCooney, R. and Cockburn, A. Anim. Behav. 1995; 49: 1635–1647Crossref | Scopus (58)See all References[3]. I agree with Eens and Pinxten that more experimental studies are needed to differentiate between the possible functions of female song. In particular, before we can conclude that female song functions for mate attraction we need to know that males can distinguish between male and female songs, and that they are preferentially attracted to female songs.