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Paleobiology, 32(1), 2006, pp. 100–108 Estimating multivariate selection gradients in the fossil record: a naticid gastropod case study Melissa Grey, Elizabeth G. Boulding, and Michael E. Brookfield Abstract.—The purpose of this paper is to explore the possibility and utility of estimating multivariate selection in fossil assemblages, using naticid gastropods as a case study. We used the presence or the absence of a naticid borehole as an index of survival with respect to drilling attacks, enabling us to estimate the multivariate selection gradient exerted by this predator on the shell length and shell thickness of two bivalve genera, Astarte and Spisula. We hypothesized that naticid selection pressure would favor the survival of large, thick-shelled bivalve prey throughout the Cenozoic. Differential survival of prey was recorded over geologic time using processed bulk assemblages from the Miocene, Pliocene, and Pleistocene Epochs. Multivariate logistic regressions were performed by time period to determine if length and thickness were important factors affecting survival. The direction and magnitude of selection on length and thickness for the two genera ranged from zero (no selection) to large positive or negative values. Only two selection coefficients were significant after sequential Bonferroni corrections: thin-shelled Astarte survived substantially better than thick-shelled Astarte during the Pleistocene (bavggrad 5 21.23) and large Spisula survived slightly better than small Spisula during the Miocene Epoch ( bavggrad 5 0.05). This is the first study using fossils to calculate multivariate selection gradients. It suggests that naticids were not necessarily strong agents of selection on two traits previously thought to be important to survival of drilling attacks for two of their common prey species. We also show that multivariate selection gradient estimates differ from traditional predation intensity estimates but are superior for estimating the magnitude and direction of natural selection because they use differential mortality of different prey phenotypes rather than just absolute mortality from predation. This work is especially significant for research that involves estimating the relative importance of predation (naticid or otherwise) as an evolutionary force and will be useful for fossil studies where differential survival can be recorded. Melissa Grey.* Department of Integrative Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada Elizabeth G. Boulding. Department of Integrative Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada. E-mail: [email protected] Michael E. Brookfield. Department of Land Resource Science, University of Guelph, Guelph, Ontario N1G 2W1, Canada * Present address: Department of Earth and Ocean Sciences, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada. E-mail: [email protected] Accepted: 4 June 2005 Introduction Understanding how natural selection affects phenotypes is a major goal of evolutionary biology, and a common theme among evolutionary neontologists is the quantification of natural selection (see Endler 1986, Kingsolver et al. 2001, and Hereford et al. 2004 for reviews). Predation is recognized as an important agent of selection and source of diversification in prey species (Vermeij 1987; Endler 1995; Reimchen and Nosil 2002). The prospect of quantifying selection due to predation for fossil assemblages is exciting because it can help elucidate how predation has shaped phenotypes throughout evolutionary history. Beq 2006 The Paleontological Society. All rights reserved. cause evidence of predation is preserved in the shells of the prey species, the naticid gastropod predator-prey system is particularly useful for exploring whether it is possible to calculate the selection intensity placed on prey by their predators over evolutionary time. Predator-driven evolution has been hypothesized for many prey taxa of naticid gastropods (e.g., Kelley 1989, 1991a; Dietl and Alexander 2000). Indeed, the increase in prey shell length and thickness for some taxa over geological time has been attributed to an evolutionary response to naticid predation (Kelley 1984, 1989). The naticid predator-prey system is an ideal 0094-8373/06/3201-0006/$1.00 101 ESTIMATING SELECTION IN FOSSILS candidate for the study of selection in the fossil record and for Recent evolutionary studies for a variety of reasons: (1) naticid predation is often stereotyped and predictable (Berg and Nishenko 1975; Kitchell et al. 1981; Kelley 1987, 1991b; Kabat 1990); (2) naticid boreholes are characteristic, preservable, and usually identifiable in prey shells (Kitchell et al. 1981; Kabat 1990); (3) boreholes in prey shells can provide a wealth of information, including predator size and predator behavior (Kitchell 1986); (4) drilling is one method of predation for which fossils can be used to estimate mortality and antipredatory effectiveness (Vermeij 1983); and (5) naticids are often assumed to be strong selective agents in prey evolution (Harper 2003). The naticid predator-prey system has been used for studies of coevolution (Kelley 1992), prey selection (Kitchell et al. 1981; Kelley 1988, 1991b), and escalation (Kelley and Hansen 1996) but no previous studies have attempted to quantify multivariate selection for this system, or for any other fossil predator-prey system. Drilling frequencies are typically used as a proxy for selection pressure due to predation (e.g., Kelley 1988, 1989; Kelley and Hansen 1993); Leighton (2002) comments that this proxy can be valid but with important caveats that he discusses. Conversely, multivariate techniques (as described below) can be used to estimate selection intensity directly. This method may be particularly important as Van Valen’s ‘‘Red Queen Hypothesis’’ (Van Valen 1973) indicates that despite evolutionary changes by the prey, predation intensities may remain nearly constant because of evolution by the predator. Predation intensity, therefore, may not always be a suitable indicator of selection pressure and more direct tests of selection pressure are required. The strength of selection is frequently calculated by using the multivariate selection gradient, which is a vector of partial regression coefficients, from a multiple regression with the various traits as the independent variables and relative fitness as the dependent variable (Lande and Arnold 1983). It is important to use multivariate methods for determining which traits in a correlated group are the focus of direct selection, as phenotypic correlations among traits are very common and natural selection acts on many characters simultaneously (Lande and Arnold 1983). Multiple regression has been widely used by researchers but logistic regression is a more suitable method for estimating the selection gradient when outcomes are dichotomous (e.g., absolute fitness recorded as survival or death) and sample sizes are relatively small (e.g., n 5 50–100) (Janzen and Stern 1998). The model for logistic regression relates the survival probability for an individual to that individual’s trait values: W(z) 5 ea01az /1 1 ea01az T T where W is the selection outcome for an individual (1 5 survival; 0 5 death); W(z) is the survival probability for a set of traits (z1 . . . zn); a 5 (a1, a2, . . . , ak)T are the logistic regression coefficients for traits (z1 . . . zn); T signifies matrix transposition; and a0 is an intercept (Janzen and Stern 1998). Although the strength of selection on quantitative traits has been estimated for numerous neontological studies, it has not hitherto been estimated for any fossil system. The purpose of this paper is to explore the possibility and utility of estimating multivariate selection gradients for fossil assemblages. We compare this method to the predation intensity statistic, which is the traditional proxy of selection for drilling predation in the fossil record. If both methods accurately estimate selection, then selection gradient estimates should be positively correlated with predation intensity (e.g., if naticids are strong selective agents on prey shell length and thickness, then selection gradients will be significant and predation intensities will be high). Our initial hypothesis was that the length and thickness of prey shells would be the most important traits affecting survival and that larger and thicker shells (Kitchell et al. 1981) will have a higher probability of surviving in the presence of naticid predators. Materials and Methods Description of Assemblages Recent. A Recent assemblage of the surf clam, Spisula (Hemimactra) solidissima, was col- 102 MELISSA GREY ET AL. TABLE 1. Information on stratigraphic unit, age, taxa, and location collected for all assemblages studied. Assemblage name Chesapeake Group (Kelley 1983) Chesapeake Group (Kelley 1983) Chesapeake Group (Kelley 1983) — — — Stratigraphic unit and members/zones Calvert Fm. (Plum Point Marl Member; zones 10 and 14) Choptank Fm. (Gernant’s Calvert Beach and Drumcliff Members; zones 16 and 17) St. Mary’s Fm. (Little Cove Point and Windmill Point Members; zones 22 and 24) Yorktown Fm. (Moore House Member) James City Fm. — Age Taxa Location collected E. Miocene Astarte cuneiformis Chesapeake Bay, Md. M. Miocene Astarte thisphila Chesapeake Bay, Md. L. Miocene Spisula (Hemimactra) subponderosa Chesapeake Bay, Md. E. Pliocene Astarte undulata and A. conheni; Spisula (Hemimactra) sp. Astarte concentrica; Spisula (Hemimactra) sp. Spisula solidissima East coast of U.S.A. E. Pleistocene Recent lected from Wrightsville Beach, North Carolina, by G. Dietl (Yale University). Wrightsville Beach is a wave-exposed sandy beach on the Atlantic Ocean. This assemblage was primarily used to compare Recent selection gradients with those of fossil assemblages, where the effects of time-averaging will have a greater effect on the magnitude of selection estimates. Fossil. Fossils used in our analyses were collected by P. H. Kelley (University of North Carolina at Wilmington) and included processed material from the Miocene, Pliocene, and Pleistocene (Table 1). Miocene assemblages were from the Chesapeake Group in Maryland and all were from an unconsolidated offshore environment (Kelley 1983, 1984). The exposures of the Chesapeake Group include sediments assigned to the Calvert, Choptank, and St. Mary’s Formations. Refer to Kelley (1983) for specific sampling techniques and a complete description of the Chesapeake Group assemblages. Plio-Pleistocene collections were from the Yorktown and James City Formations, respectively. Bivalve genera studied were Astarte and Spisula; these were the most common genera present from the Miocene and traceable through to the Plio-Pleistocene. Following Kel- East coast of U.S.A. Wrightsville Beach, N.C. ley (1983), we assume that, at least for Astarte, the lineages studied represent true ancestordescendant relationships in the Chesapeake Group. The naticid species found in these assemblages include Neverita duplicata (Say) and Euspira heros (Say). Table 1 contains information on the biostratigraphy, taxa, and age for all assemblages studied. Measurements We measured two traits, length and thickness, that are expected to have adaptive value, as indicated by previous studies of naticid gastropod predation on bivalves (Kitchell et al. 1981; Roopnarine and Beussink 1999). All shells were measured for maximum length with digital calipers. Thickness measurements on the shells, made with a digital depth gauge, were taken in the regions of the umbo (corresponding to sector 2 in Kelley [1988]), middle (corresponding to sector 5 in Kelley 1988), and edge (corresponding to sector 8 in Kelley 1988). Overall thickness of a shell was calculated as an average of the thickness at the umbo, middle, and edge regions. All measurements were taken to the nearest 0.01 mm and were entered into a customized database 103 ESTIMATING SELECTION IN FOSSILS TABLE 2. Overall multivariate logistic regression results for Astarte from the Miocene to the Pleistocene. n is the number of bivalves measured in the assemblage; bavggrad is the transformed logistic regression coefficient; p is the original value before correction for multiple tests within each epoch; and SE is the standard error. Analyses used fitness (drilled versus undrilled) as the dependent variable and length and thickness as the independent variables. bavggrad p SE Epoch n Predation intensity (%) Length Thickness Length Thickness Length Thickness Miocene Pliocene Pleistocene 58 51 50 76 71 48 0.007 0.06 0.1 20.09 20.46 21.23 0.64 0.07 0.03 0.60 0.09 0.03† 0.06 0.35 0.25 0.7 3.5 3.6 † Remained significant after the sequential Bonferroni correction within each epoch (Rice 1989). using an automatic data acquisition program, written in FoxPro. Predation Intensity and Selection Gradients for Fossil Assemblages Overall predation intensity for each time period was calculated by 2(D/N) where D is the number of drilled valves and N is the total number of valves (Thomas 1976). Multivariate logistic regressions were performed in SPSS for both Astarte and Spisula by time period. Absolute fitness (survival 5 1; death by drilling 5 0) was the dependent variable (Janzen and Stern 1998) and prey shell length and thickness were independent variables. Each selection episode, or time period in this case, has been treated as a separate experiment, after Fairbairn and Reeve (2001). We present results for significant levels corrected for multiple comparisons using the sequential Bonferroni method (Rice 1989) within each epoch, thus maintaining an experimentwise error of alpha 5 0.05. Unlike the standard Bonferroni test, the sequential Bonferroni method retains statistical power while correcting for experimentwise Type I error (Rice 1989). Logistic regression coefficients were con- verted into least-squares selection gradients (as in Lande and Arnold 1983) using the methods described by Janzen and Stern (1998). Conversion of the coefficients results in the average gradient vector (bavggrad) and requires calculating W(z) for each individual (Janzen and Stern 1998). These calculations were performed using a program created by P. Lelièvre in MatLab. Results Predation intensities decreased from 76% to 48% from the Miocene to Pleistocene (Table 2) for Astarte and decreased from 80% to 40% for Spisula from the Miocene to Recent (Table 3). Logistic regression results by time period revealed that length and thickness did not usually affect the probability of being drilled for Astarte (p . 0.25 for two out of six tests; Table 2) or for Spisula (p . 0.25 for five out of eight tests; Table 3). However, the test for thickness for Astarte concentrica during the Pleistocene was significant after the sequential Bonferroni correction (p 5 0.03) and this result corresponded to a highly negative selection gradient value (bavggrad 5 21.23) (Table 2, Fig. 1), indicating selection for thinner shells. Also, one test for length for Spisula during the TABLE 3. Overall multivariate logistic regression results for Spisula from the Miocene to the Pleistocene. n is the number of bivalves measured in the assemblage; bavggrad is the transformed logistic regression coefficient; p is the original value before correction for multiple tests within each epoch; and SE is the standard error. Analyses used fitness (drilled or undrilled) as the dependent variable and length and thickness as the independent variables. Epoch n Predation intensity (%) Miocene Pliocene Pleistocene Recent 147 147 80 111 80 53 30 40 bavggrad p SE Length Thickness Length Thickness Length Thickness 0.05 0.002 0.005 0.005 0.17 0.24 0.11 0.31 0.01† 0.89 0.54 0.10 0.82 0.31 0.77 0.10 0.09 0.06 0.11 0.05 5.2 1.2 3.3 2.9 † Remained significant after the sequential Bonferroni correction (Rice 1989). 104 MELISSA GREY ET AL. FIGURE 1. Length-thickness graph for Astarte shells unbored and bored by naticids in the Pleistocene Epoch. Late Miocene was significant (p 5 0.01) after the sequential Bonferroni correction but this result corresponded to a very small selection gradient value (bavggrad 5 0.05) (Table 3, Fig. 2), indicating weak selection for larger shells. Refer to the Appendix for number of bored shells sampled and trait means and standard deviations. Selection intensity and predation intensity were inversely correlated for Astarte and were positively correlated for Spisula (Tables 2 and 3, respectively, Fig. 3). Discussion Logistic regression analyses indicated that length and thickness, two traits often assumed to be important to survival, did not usually significantly affect the probability of finding naticid drill holes in Astarte and Spisula. We have also shown that high predation intensities do not always correlate with strong selection. As we discuss below, these results indicate that 1. predation intensity may not always be an appropriate proxy for selection; or 2. the traits measured (length and thickness) were not experiencing selection pressure from naticids and were not important factors to survival. Therefore, attributing temporal increases in thickness and/or length in prey shells to naticid predation is not valid unless there is direct evidence; or 3. selection has not been measured in an appropriate manner. Predation intensity may not always be an appropriate proxy for selection because it es- FIGURE 2. Length-thickness graph for Spisula shells unbored and bored by naticids from the St. Mary’s Formation in the Miocene Epoch. timates absolute mortality from predation rather than differential mortality of different prey phenotypes. Predation intensity, as defined here, measures the percentage of bivalve valves of a particular species that were drilled by naticid predators without any reference to shell traits. In contrast, a selection gradient estimates the covariance between the values of shell length and shell thickness and whether or not a naticid predator drilled the shell. This differential survival with respect to particular values of prey traits is important as only it can result in natural selection and ultimately evolution of heritable traits (reviewed in Endler 1986). It is possible that neither length nor thickness was experiencing strong selection during these time periods but our values are comparable to those for Recent populations. Absolute values of linear selection zbavggradz for this study averaged 0.20 (range 5 0.002–1.23, for length and thickness results combined). This is comparable to the mean value of 0.22 for other studies of natural selection for a variety FIGURE 3. Relationship between selection coefficients and predation intensities for Astarte and Spisula. ESTIMATING SELECTION IN FOSSILS of Recent populations (Kingsolver et al. 2001). In addition, we found that 21% of estimates were significant (14% after the sequential Bonferroni correction), similar to the Kingsolver et al. (2001) review of 63 published studies that found significance in 25% of all estimates of selection (where corrections for multiple tests were not normally calculated). Selection strength was very small (bavggrad 5 0.05) for Spisula during the Miocene Epoch for increased length. Even very small selection coefficients, however, can have large evolutionary effects over geologic time (Lande 1979). It is intriguing that selection has sometimes been weak or nonsignificant on these two common prey genera because naticids and other drilling gastropods are often assumed to have placed significant selection pressure on their prey (Harper 2003). Future research will need to discern between two, ultimately testable, hypotheses: that selection pressure by naticids is weak and is not the primary factor for observed bivalve morphological evolution or that the methods used here are not suitable for evaluating selection. A common reason for not detecting selection is that sample sizes are too small (Endler 1986). Although logistic regression works well with relatively small sample sizes, the power of the analysis may increase with larger sample sizes (Kingsolver et al. 2001) and we recommend that sample sizes be maximized for work involving the calculation of selection gradients. This study is based on four assumptions that may have substantially affected our interpretations and will be described below. Note that the importance of non-facultative predation is not discussed here because it does not affect questions relating to the importance of naticids as drilling predators. Taphonomic bias in assemblages can hinder analyses as some predation events can be lost. For example, differential fragmentation (Roy et al. 1994) and valve sorting (Boucot et al. 1958; Lever and Thijssen 1968) may eliminate a portion of drilled shells from assemblages. Although the presence of boreholes in shells significantly reduces shell strength, shell-toshell contact has a greater effect on valve breakage (Zuschin and Stanton 2001). Even 105 though quantifying selection does not rely on estimating frequencies, differential fragmentation may have affected our results. For instance, the observed strong negative selection (bavggrad 5 21.23) for Astarte during the Pleistocene suggests that thinner-shelled prey survived better than thick-shelled prey and may be a result of differential fragmentation; thinner shells may have been removed from assemblages, representing a severe taphonomic bias. This may have been a real trend, however, as all the selection coefficients for shell thickness were negative for Astarte for all geological epochs whereas all were positive for Spisula. Roy et al. (1994) presented a method for assessing the amount of taphonomic loss in fossil assemblages, but because we used previously processed and published material (see Kelley 1983) we were not able to assess the extent of the bias. The development of probabilistic models to account for taphonomic loss and multiple hypotheses testing as advocated by Kaplan and Baumiller (2000) should also be considered when estimating selection intensities. The destruction of bivalve shells by crabs and other shell-breaking predators (Vermeij et al. 1989) may have also affected our results. Valve destruction will be of major concern for this study if large removals of bivalves with specific characteristics (e.g., thin and/or small) took place. Removals could account for the observed negative selection gradient for Astarte only if crabs differentially removed thicker shells from the record, but crabs prefer thinner and flatter shells (Boulding 1984). As mentioned earlier, the assemblages we worked with had already been processed and the magnitude of fragmentation could not be judged. Future studies, however, can assess crab predation by using the relative abundance of shell fragments with angular (Oij et al. 2003) or chipped ventral margins (Boulding 1984). Valve destruction is of much greater concern for drilling intensity statistics because it will overestimate the importance of drillers. Taphonomic alteration, among other factors, can affect the geometry of a drill hole (Kowalewski 1993), causing the source of predatory holes to be misidentified. We do not believe that there were many misidentified 106 MELISSA GREY ET AL. holes in this study because preservation was satisfactory. For assemblages where concerns about this assumption are high, Kowalewski (1993) has presented a method for a morphometric analysis of drillholes. Time-averaging is another important issue that must be addressed as it can mask intense bouts of selection over time. Our results for the Recent assemblage of Spisula closely match those for fossil assemblages, and our overall results are similar to published material on Recent populations (Kingsolver et al. 2001). We are therefore confident that our results are reasonably accurate; however, time-averaging remains an important issue that will require further attention as research in this area continues. Although violation of these assumptions affects the utility of calculating selection gradients, we feel there is vast potential for this method to be applied in paleobiological studies involving predation, and natural selection in general. Future research on this system should include additional prey taxa and traits, such as internal volume (see Kelley 1989), that may have adaptive value and are likely to be heritable. Our methods will be most valuable for assemblages for which many of the assumptions above can be met. For many unprocessed fossil assemblages it should be possible to minimize the number of assumptions and create a powerful test for estimating multivariate selection. For results that are not statistically significant, choosing between the alternative hypotheses—that selection pressure is not strong or that the specimens/variables/ sampling methods are not suitable—should pose an interesting challenge to paleobiologists. Researchers of drilling predation may consider using incomplete boreholes in prey as a measure of unsuccessful predation. Prey with unsuccessful boreholes would receive a fitness value of one, whereas prey with complete boreholes would receive a value of 0. We were unable to perform this because the incidence of incomplete holes in our samples was extremely low (5%) and would not allow for reasonable statistical power. Also, many examples from modern drilling systems indicate that an incomplete borehole may not result in failed predation (for naticids, see Vermeij 1980, Ansell and Morton 1987, and Grey 2001; for muricids, see Kowalewski 2004). It is also important to recognize that a naticid may have encountered a prey item but did not attempt to drill it because of its particular traits, representing a form of prey selection that would be ignored if only incomplete holes were used as a measure of survival. Comparing selection coefficients that use only incomplete boreholes as a measure of survival with results that use all undrilled shells may prove useful for determining which method is most appropriate. Conclusions The importance and role of natural selection in evolution has been the subject of numerous studies by neontologists, but has never before been estimated for fossils. We have shown it is possible to measure the strength of selection for fossil predator-prey systems, noting important caveats for interpretation. This paper represents a growing body of research that aims to directly assess predation pressure in the fossil record (e.g., Harper 2003; Gahn and Baumiller 2005; Grey et al. 2005). The methods presented here are useful not only for assessments of drilling predation but also for any fossil system where differential survival can be recorded. Our paper highlights four important points: 1. multivariate selection can be quantified for fossil assemblages; 2. naticids may not be important selective agents on bivalve evolution, as often assumed, or bivalve thickness and length traits may not be important to survival, as often assumed; 3. predation and selection intensities are not always positively correlated (Fig. 3), indicating either that predation intensities cannot always be a useful measure of selective pressure or that selection gradients are not accurately estimated; and 4. the most powerful tests for multivariate selection will include comparisons of drilling intensities with selection gradients in fossil assemblages that are well preserved, with minimal taphonomic biases. ESTIMATING SELECTION IN FOSSILS Estimation of selection in the fossil record is an exciting prospect as it can help us further understand the role of predation as a selective force and recognize how natural selection has affected morphological evolution in the past. We hope that this work will encourage researchers to use and further develop the methods we describe here to estimate selection in the fossil record. Acknowledgments This research was funded by a Discovery grant to E. G. Boulding and by a Post-Graduate Scholarship-A to M. Grey from the Natural Sciences and Engineering Research Council of Canada. We thank J. W. Haggart for reading early drafts of this manuscript, P. G. Lelièvre for creating a program in MatLab, T. K. Hay for writing a custom database program, and especially G. P. Dietl and P. H. Kelley for the extensive use of their collections. This manuscript has been significantly improved by helpful comments from T. K. Baumiller and reviews by G. P. Dietl, P. H. 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