| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1 Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, California 95039
2 Department of Biology, 101 Hurst Hall, American University, 4400 Massachusetts Avenue, NW, Washington, DC 20016-8007
* To whom correspondence should be addressed. E-mail: bseibel{at}mbari.org
Metabolic rates of deep-living animals have been intensely studied (1). Within pelagic fishes, crustaceans, and cephalopods, a strong decline in rates of mass-specific metabolism with depth has been observed. Childress and Mickel (2) put forward the visual interactions hypothesis to explain this general pattern. Their hypothesis states that reduced metabolic rates among many deep-sea pelagic taxonomic groups result from relaxed selection for strong locomotory abilities for visual predator-prey interactions in the light-limited deep sea. This pattern has, however, been tested using mean metabolic rates for species as individual data points. Felsenstein (3) warned that, because species are descended in a hierarchical fashion from common ancestors, they generally cannot be considered as independent data points in statistical analyses. Statistical methods have recently been developed that incorporate phylogenetic information into comparative studies to create phylogenetically independent values that can then be used in statistical analyses. Reliable independent phylogenetic information has only recently become available for some deep-sea organisms. The present contribution reanalyzed the metabolic rates (4,5) of pelagic cephalopods as a function of, for consistency with previous studies, MDO (minimum depth of occurrence) using phylogenetic independent contrasts derived from a recent molecular phylogeny (6). This analysis confirms the existence of a significant negative relationship between metabolism and minimum habitat depth in pelagic cephalopods but suggests that phylogenetic history also has considerable influence on the metabolic rates of individual species.
Childress (1) argued against a phylogenetic basis for the observed relationships between metabolism and depth. He based the argument on the identification of convergence of metabolic rates at a given depth among distantly related taxa (fishes, crustaceans, cephalopods) as well as divergence within closely related groups as a function of depth. This pattern strongly suggests that species experience similar selective regimes at any given depth and that rates of metabolism are evolved in response to that selection. Seibel et al. (5) further argued, on the basis of an analysis of higher nodes, that most of the variation in metabolic rates among cephalopods is between families within an order, as opposed to between genera within a family or species within a genus. Therefore, families are more appropriate units for comparison. A decline in metabolic rates with increasing habitat depth was also observed when families were used as independent data points (5). Nevertheless, the degrees of freedom used for statistical analyses in these studies are elevated, to varying degrees, due to phylogenetic non-independence of the data.
Felsenstein (3) proposed computing weighted differences ("contrasts") between the character values of pairs of sister species nodes, or both, as indicated by phylogenetic topology, thereby estimating an ancestral character value (e.g., the ancestral states of log-transformed depth and metabolic data presented in Fig. 1). Insofar as the ancestral nodes are correctly determined, each of these contrasts is independent of the others in terms of the evolutionary changes that have occurred to produce differences between the two members of a single contrast (7). Felsenstein’s (3) method requires knowledge of the cladistic relationships between the species being analyzed. Several studies have attempted to construct phylogenies for cephalopods. However, only a single reliable family-level phylogeny exists that includes deep-water fauna. One previous phylogenetic analysis relied exclusively on morphological characters that are associated with buoyancy and locomotion and are thus confounded with metabolism and depth (8). We therefore felt that analysis was unsuitable for use in the present study. Other analyses have been unable to obtain sufficient resolution for familial relationships (9) or have included only shallow-living taxa (10,11). Carlini and Graves (6) recently analyzed the higher level phylogenetic relationships of extant cephalopods by using a 657-bp sequence of the mitochondrial cytochrome c oxidase (COI) gene. The molecular sequence data from Carlini and Graves (6) provide an opportunity to test the visual interactions hypothesis directly, using a more valid statistical approach. An additional analysis based on actin gene sequences (12) was not included, primarily because there was very little overlap between taxa for which actin gene sequences were available and those for which metabolic data are available. Furthermore, the actin study provides a more accurate reconstruction of gene family evolution within the cephalopods than of specific relationships among taxa.
|
A second requirement of Felsenstein’s (3) method is knowledge of branch lengths in units of expected variance of change. Ideally, branch lengths should represent expected units of evolutionary change (gradual model). For this approach to be valid, independent contrasts must be adequately standardized so that they will receive equal weighting in subsequent regression analyses. We plotted the absolute value of each standardized independent contrast, generated from the fully resolved tree (Fig. 1a), versus its standard deviation (7) and found no relationship between the two variates (data not shown). Thus, the contrasts were adequately standardized and properly weighted in regression analysis.
However, even if a particular phylogenetic tree is well resolved and well supported, branch lengths are always estimates and are thus subject to error. A less optimal approach, but one that involves fewer assumptions about the evolutionary relationships of the taxa in question, is to assume that every branch in the phylogeny is the same length (punctuated model). The advantage of this approach is that it can be used for poorly resolved trees or for data sets where branch lengths cannot be estimated, such as those derived from both molecular (6) and morphological (13,14) data. This allows more contrasts to be performed, increasing the power of subsequent statistical tests. On the other hand, the punctuated model is unrealistic for most data sets, as there is likely to be significant heterogeneity with respect to the evolutionary rates of the taxa under study. In any case, use of a punctuated model is far superior to any method that treats species values as independent data points.
In the present study we employed both gradual and punctuated models in constructing trees for comparison. The gradual model tree is depicted in Figure 1a (21 taxa, metabolic rates as a function of MDO). A similar tree was constructed including species for which enzymatic data are available (not shown, 18 taxa, enzymatic activities as a function of MDO). A tree constructed using the punctuated model for contrasts involving all taxa for which data are available is depicted in Figure 1b (39 taxa, metabolic rates versus MDO). A similar tree was constructed including species for which enzymatic data are available (not shown, 32 taxa, enzymatic activities versus MDO).
Independent contrasts for log-transformed, normalized mean oxygen consumption rates (4,15–18) were produced, for both gradual and punctuated models, using CAIC v. 2.0.0 (19), and were regressed against those produced for MDO (Fig. 2, Table 1). We produced similar regressions for contrasts of activities of citrate synthase (CS) and octopine dehydrogenase (ODH) (5,20–22), indicators of aerobic and anaerobic metabolic potential, respectively (Table 1). We tested the validity of log transformation by using a method suggested by Purvis and Rambaut (19), authors of the CAIC package. Regressions of the absolute values of the contrasts on the estimated nodal values were performed, and none had slopes significantly different from zero. We also performed regressions of the absolute values of the contrasts against the standard deviations of the contrasts and detected no relationship in any case. These two tests ensure that we did not violate any of the assumptions of Felsenstein’s (3) model of evolution of continuous characters as a random walk process.
|
|
Although these results suggest a negative trend in metabolism with increasing depth independent of phylogeny, there are clearly phylogenetic influences on the data. For example, members of the family Cranchiidae (including Cranchia and Liocranchia, the contrast excluded from several of the analyses) have low metabolic rates regardless of habitat depth. The Cranchiidae is a very diverse family, and our data set is slightly biased toward cranchiid species (n = 7 out of 39, MO2, punctuated model, Fig. 1b). Although many cranchiid species undergo ontogenetic vertical migrations in which successive developmental stages occupy progressively greater depths (12,23), some species appear to remain near the surface until sexual maturity (24,25). Seibel et al. (4) argued that the use of transparency (26) by the cranchiids reduces detection distances (27) at all depths and therefore allows them to employ sit-and-wait predation strategies, facilitating low metabolic rates, even in well-lit epipelagic waters. With the Cranchia-Liocranchia contrast removed, we consistently observed a much stronger relationship between metabolism and habitat depth. Several sources of depth-related variation in metabolism, such as buoyancy and body mass, exist in addition to phylogeny. These have been discussed elsewhere (4,5).
 |
Footnotes |
|---|
|
Literature Cited |
|---|
 TOP Literature Cited |
|---|
This article has been cited by other articles:
|
|
 |
|
  B. A Seibel and J. C Drazen The rate of metabolism in marine animals: environmental constraints, ecological demands and energetic opportunities Phil Trans R Soc B, November 29, 2007; 362(1487): 2061 - 2078. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B. A. Seibel On the depth and scale of metabolic rate variation: scaling of oxygen consumption rates and enzymatic activity in the Class Cephalopoda (Mollusca) J. Exp. Biol., January 1, 2007; 210(1): 1 - 11. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
