Ectocion Phylogeny

Phylogenetic relationships reconstructed within Ectocion (Fig. 1) are largely concordant with the interpretation that Thewissen (Reference Thewissen1992) derived from the same dataset based on stratocladistic criteria. The main point of contention lies in the placement of Ectocion mediotuber Thewissen, Reference Thewissen1990 and Ectocion cedrus Thewissen, Reference Thewissen1990 in relation to Ectocion collinus Russell, Reference Russell1929. The original study suggested the three taxa form a grade, separated by hypothetical ancestors, whereas the current reconstruction posits that E. cedrus and E. mediotuber independently budded from E. collinus. This is a minor difference that will be discussed further later in the paper. Otherwise, the ancestor–descendant linking of E. mediotuber to Ectocion osbornianus Cope, Reference Cope1882 and Ectocion parvus Granger, Reference Granger, Matthew and Granger1915 corresponds identically to the original study. Thewissen was conservative in his interpretation of Ectocion superstes Granger, Reference Granger, Matthew and Granger1915. However, the approach here suggested that it may have speciated from E. osbornianus. It should be noted that, while the diagram presented here gives the appearance of a direct ancestor–descendant relationship between the two, it is very possible that their true genealogical relationship is separated by one or more unobserved species. This would still make E. osbornianus an indirect ancestor.

Figure 1. Reconstructed ancestor–descendant relationships within Ectocion. Bars represent stratigraphic ranges. Dotted lines indicate genealogical relationship between ancestral and descendant lineages. Colors reflect presence or absence of the metacone on the P3. Inset phylogeny represents hypothetical alternative reconstruction that better accommodates pattern in the evolution of P3 polymorphism. Further evaluation would be needed to distinguish between these two. Timescale reflects the discrete zonation used by Thewissen (Reference Thewissen1992).

Evolution of the P3 Metacone Polymorphism

Mapping the evolution of the P3 metacone to the Ectocion phylogeny illustrates the importance of considering both ancestor–descendant relationships and polymorphism when reconstructing patterns in morphological evolution in the fossil record. A standard cladogram would fail to capture how polymorphisms in E. mediotuber and E. osbornianus persisted and sorted among the respective descendants of each, instead representing the pattern of character changes through multiple character reversals. One slightly confusing pattern in P3 metacone evolution is the apparent sudden emergence of a monomorphic metacone in E. cedrus. A more parsimonious interpretation, based on P3 morphology, of the sequence of lineage divergence than that achieved using the greedy method implemented here is given in the inset to Figure 1, which implies that the metacone evolved one time and sorted among descendant lineages while being maintained across multiple species. Alternatively, it is possible that the metacone truly did evolve twice in Ectocion. A stronger understanding of the developmental programs controlling dental variation would help to distinguish whether the metacone is sufficiently evolvable to have emerged twice, but distinguishing between these two possibilities falls outside the scope of this study. While the invocation of an additional, unaccounted polymorphic hypothetical ancestor provides a better explanation for P3 morphology evolution, detailed phylogenetic work that more thoroughly explores treespace using parsimony or probabilistic criteria will be needed to confidently distinguish between these possibilities.

Distinguishing between inheritance of ancestral polymorphism and character reversal is important for deriving meaningful biological interpretations. The pattern in P3 evolution reconstructed here is consistent with a scenario in which balancing selection maintains variation across a long-lived lineage, giving rise to descendant lineages that fix that ancestral variation in different ways. If the maintenance of polymorphism by balancing selection is as common as ecological theory might suggest, many character distributions among fossil taxa (which are often interpreted as being highly homoplasious) may simply be driven by the sorting of variation among a small handful of variable ancestral lineages. In addition to potentially helping solve problems in paleontological systematics, exploration of these dynamics may shed light on the processes that drive the diversification of clades over paleobiological timescales.

The persistence of the P3 metacone polymorphism across E. mediotuber and E. osbornianus over several million years is difficult to explain by genetic drift alone. While some fluctuation was observed in the character state frequency throughout the range of E. osbornianus, the polymorphism remained at reasonably intermediate frequency, with >30% and <60% of individuals displaying the metacone throughout the duration of the lineage (Thewissen Reference Thewissen1992). NFDS provides one possible explanation for this maintenance. Competition for food resources could provide negative, frequency-dependent feedback on the frequency of each P3 morph if metacone presence yielded different fitness outcomes related to the processing of some limiting food resource as a function of population density. Several modes of competition have long been recognized as an important cause of NFDS (Antonovics and Kareiva Reference Antonovics and Kareiva1988; Dijkstra and Border Reference Dijkstra and Border2018). The most relevant mode for P3 morphology might be resource competition associated with density dependence. Alternatively, the persistence of the P3 polymorphism might instead result from some form of bet-hedging or response to soft selection in the presence of environmental heterogeneity over either space or time. At least equally likely is the possibility that P3 morphology is selectively neutral and fluctuated in frequency due to genetic drift. Whatever maintained this polymorphism, the results here demonstrate how sorting from ancestral stock shapes the phenotypes displayed by incipient descendant lineages. The fixation of monomorphic P3 forms in the descendant lineages E. major, E. parvus, and E. superstes reflects either adaptation or drift from standing variation present in the ancestral lineages. If some form of balancing selection maintained P3 polymorphism in E. mediotuber and E. osbornianus, it is possible that demographic bottlenecks encountered during speciation of the three descendant lineages led to random fixation. More exploration into the overall levels of phenotypic diversity and geography of these descendant lineages would help to examine the feasibility of this explanation.

Barycrinus Phylogeny

Throughout its evolutionary history, Barycrinus displayed several long-lived lineages that gave rise to more than one descendant (Fig. 2). In particular, Barycrinus rhombiferus is identified as having been a highly prolific lineage, with four immediate descendants. This is consistent with its status in Gahn and Kammer's (Reference Gahn and Kammer2002) analysis, which found the placement of B. rhombiferus to be highly uncertain, leading the authors to identify the lineage as a “rogue taxon.” The authors interpreted this to suggest that this uncertainty may have resulted from B. rhombiferus having itself given rise to multiple later-occurring Barycrinus lineages. Based on patterns in the inheritance of ancestral character states, Gahn and Kammer suggested that B. rhombiferus was likely the direct ancestor of Barycrinus magister Hall, Reference Hall1858, Barycrinus spectabilis Meek and Worthen, Reference Meek and Worthen1870, and Barycrinus scitulus Meek and Worthen, Reference Meek and Worthen1860—an assertion that was further supported by Gahn (Reference Gahn2003). They also suggested a possible close link between B. rhombiferus and Barycrinus spurius, going on to speculate that B. rhombiferus may be ancestral to most other Barycrinus lineages. Nevertheless, Gahn and Kammer's analysis, which was relied only on traditional cladistic methods, achieved only low resolution, perhaps due to both the rampant polymorphism and the complex pattern of ancestor–descendant relationships found in the clade. The phylogenetic tree recovered here is also largely consistent with quantitative results achieved using stratocladistics (F. Gahn personal communication 2003) and Bayesian methods (D. Wright personal communication 2022).

Figure 2. Phylogeny of Barycrinus. Bars represent stratigraphic ranges. Dotted lines indicate genealogical relationship between ancestral and descendant lineages. Width of stratigraphic lines represents scaled number of polymorphisms—a measure of genetic variation within each lineage. Shading represents the proportion of character states displayed by each lineage that were also possessed by its ancestor. Timescale approximates the discrete stratigraphic units used by Gahn and Kammer (Reference Gahn and Kammer2002).

Barycrinus underwent a rapid radiation while drawing upon a stock of ancestral variation maintained by B. rhombiferus and, to a lesser extent, B. spurius. This dynamic provides a small-scale demonstration of how the filtering of phenotypic variation during speciation might shape patterns at deeper timescales. In the phylogenetic analysis presented here, B. rhombiferus is depicted as having given rise to four descendant lineages. Two of these, B. spectabilis and B. scitulus, displayed a small fraction of the variation displayed by their ancestor as well as significantly reduced durations. If both of these incipient lineages occupied the same ecological landscape as B. rhombiferus, they may have been at a competitive disadvantage (at the lineage level), which would explain their shorter durations. The high phenotypic variability displayed by B. rhombiferus could stem from environmental heterogeneity caused by broader niche occupancy. If so, the increased survivorship displayed by generalist crinoids (Kammer et al. Reference Kammer, Baumiller and Ausich1997; Cole Reference Cole2021) might be explained by increased bet-hedging capability displayed by generalists that are able to maintain pools of phenotypic variation. Alternatively, if functional interpretations for the traits that are polymorphic in B. rhombiferus are more consistent with non-adaptive explanations (as may be the case; F. Gahn personal communication 2023), it is possible that its high variability simply stems from its increased ability to acquire (and subsequently maintain) variation over its long duration (M. Foote personal communication 2023). This explanation would require a scenario wherein mutation and genetic drift cooperate to introduce and maintain neutral variation over geologic timescales.

Barycrinus magister and B. spurius experienced longer durations than their siblings. This could be explained in B. magister by its evolution of additional derived character states not present in B. rhombiferus, which may be indicative of an escape to distinct ecological conditions. However, this scenario cannot be evaluated at present due to the geographic co-occurrence of both lineages and the lack of complete stem preservation in B. magister (F. Gahn personal communication 2023). While crinoids, as generalist suspension feeders, often occupy very similar ecological niches, a spectrum of niche differentiation does exist (Ausich Reference Ausich1980; Ausich and Bottjer Reference Ausich and Bottjer1982). The extended duration and multiple speciations produced by B. spurius might be explained by its continued maintenance of much of the variation possessed by B. rhombiferus as well as its derivation of several new characters. These possibilities remain speculative within the context of this article; however, they may be fruitfully explored as hypotheses to be tested in future work that includes more comprehensive ecological information that can be compared against functional morphological reconstructions. Evaluating the ideas presented here in light of such additional information may help to more rigorously explain the distinct causes underlying the patterns of lineage persistence and morphological variation displayed by Barycrinus. The analysis here represents a starting point from which to draw deeper links between the evolution of phenotypic variation across species bounds and the ecological strategies employed by crinoid species.

Random versus Adaptive Sorting of Ancestral Variation

The process of budding speciation, as typically conceived, may often yield population bottlenecks. If the bottleneck is strong enough, different character states would be expected to fix when small subpopulations are drawn from polymorphic ancestral populations over repeated trials (Fig. 3A). Alternatively, sufficiently strong positive selection would fix the same character state over repeated trials if incipient lineages repeatedly move out of the ancestral niche and into the same derived niche (Fig. 3B). I leveraged the repeated budding speciations displayed across Barycrinus to identify whether ancestral variation tended to sort randomly (Fig. 3A) or adaptively (Fig. 3B). Based on the permutation tests, it was not possible to distinguish the pattern by which the descendants of B. rhombiferus and B. spurius sorted and fixed variation from their respective ancestors from the expectation under drift induced by bottlenecking (Tables 1 and 2). None of the pairs of descendants of either lineage showed statistically significant signs of parallel or divergent speciation. Nevertheless, B. spectabilis and B. magister were somewhat more similar than expected under random sorting, while B. spectabilis and B. spurius were more divergent than expected. The lack of significance could be a consequence of the small pool of traits included in this dataset, so further tests are needed to see whether more comprehensive phenotypic sampling would distinguish the observed patterns from drift.

Figure 3. Distribution of simulated allelic frequencies over 10 replicated populations while a balanced ancestral polymorphism is filtered into a budding descendant under two different adaptive scenarios: A, Polymorphism maintained by negative frequency dependent selection (NFDS) in a large ancestral population that becomes randomly fixed in bottlenecking encountered during budding speciation. B) Polymorphism maintained by NFDS that becomes fixed due to positive selection (PS) in a budding descendant that has dispersed into a new environment. Lineage widths in budding lineage diagrams represent effective population size. Under scenario A, variation is filtered randomly by drift into the descendant lineages. Under scenario B, the new regime rapidly fixes one allele/character state according to its new selective landscape.

Table 1. Pairwise phenotypic distances calculated among characters sorted from polymorphisms present in the ancestor, Barycrinus rhombiferus, between descendant lineages, relative to null expectation generated under random sorting of ancestral polymorphisms. No pairs were statistically significant at the 2.5% threshold.

Table 2. Pairwise phenotypic distances calculated among characters sorted from polymorphisms present in the ancestor, Barycrinus spectabilis, between descendant lineages, relative to null expectation generated under random sorting of ancestral polymorphisms. No pairs were statistically significant at the 2.5% threshold.

Throughout the radiation of Barycrinus, variation maintained within ancestral lineages filtered down through a series of successively less variable descendants (Fig. 2). The only exceptions lie in the emergence of B. rhombiferus from Costalocrinus ibericus Kammer, Reference Kammer2001 and Costalocrinus rex McIntosh, Reference McIntosh1984 from the hypothetical descendant of C. ibericus. The sudden and almost coincident emergence of high phenotypic variability in B. rhombiferus and C. rex from the monomorphic C. ibericus can be explained by a difference in sample size. Costalocrinus ibericus is known only from a single specimen (Kammer Reference Kammer2001), so the true extent of intraspecific variation that originated across this transition cannot be evaluated from the data used here. The descendants of polymorphic ancestors are universally less variable than their ancestors. In all, seven total lineages formed across Barycrinus by filtering variation maintained over millions of years by B. rhombiferus and B. spurius. While some of the variation displayed by B. rhombiferus may not have persisted over its entire range, the lineage did maintain high levels of polymorphism throughout its existence. Each descendant lineage that budded from B. rhombiferus and B. spurius might be characterized as a unique natural experiment, randomly fixing ancestral variation and either persisting or perishing in its new habitat. More ecological information would be needed to understand the specific phenotypic determinants of persistence and extinction among the varied Barycrinus offspring lineages.

A Brief Note on Speciation Mode

The phylogenetic results in both Ectocion and Barycrinus reveal a pattern of extensive budding speciation. The relative frequency of alternative speciation modes in the fossil record is still not well known. Researchers have dealt with this uncertainty through a range of approaches. Some studies have explored patterns across a range of potential modes (Foote Reference Foote1996), others have assumed budding a priori (Raup and Gould Reference Raup and Gould1974; Van Valen Reference Van Valen1975; Raup Reference Raup1985), and still others have resorted to the use of cladograms, which make no assumptions about mode, at the cost of evolutionary specificity. Nevertheless, several studies have examined the frequency of modes across lineages. In general, anagenesis is thought to be rare relative to budding, occurring in a small minority of cases at one extreme (2%; Bapst and Hopkins Reference Bapst and Hopkins2017) and in a larger minority at another (25%; Archibald Reference Archibald1993). Another important study found budding to form the predominant speciation pattern, with both anagenesis and bifurcating cladogenesis providing poor explanations for phylogenetic patterns in the fossil record (Wagner and Erwin Reference Wagner, Erwin and Anstey1995). Here, I assume that budding speciation forms the predominant pattern in both lineages analyzed, while also allowing for the potential of both bifurcating cladogenesis and anagenesis. The potential for anagenesis appears quite low across both datasets, with only three candidate anagenetic ancestor–descendant species pairs: E. osbornianus–E. superstes, Barycrinus stellatus Hall, Reference Hall1858–Barycrinus punctus Feldman, Reference Feldman1989, and B. rhombiferus–B. spectabilis, due to their non-overlapping ranges. Each of these three species transitions could be explained by either anagenesis or budding. The results recovered here are robust to a small handful of anagenetic transitions, with only minor modifications of the interpretation of the demographic processes underlying ancestral (pseudo-)extinction and descendant speciation. The general result that ancestors tend to be more variable than descendants and that ancestral variation tends to sort randomly into descendants would also remain intact.

Phenotypic Variation, Geographic Range, and Lineage Duration

The pattern uncovered here of long-lived, variable ancestors giving rise to multiple, shorter-lived, less variable descendants may be reflective of a more general phenomenon. Barycrinus rhombiferus, which gave rise to multiple descendant lineages over a long duration, was phenotypically variable, geographically widespread, and highly abundant (Gahn and Kammer Reference Gahn and Kammer2002). The finding that descendant lineages displayed lower phenotypic variation is not surprising, given that they were also more geographically constrained and fewer in number than their ancestor. This is consistent with the demographic asymmetry associated with budding speciation and the peripheral geographic isolation expected under peripatric speciation (Mayr Reference Mayr1963). As a result, the pattern uncovered here highlights the potential role geography may play in shaping both patterns in lineage survivorship and the origin and maintenance of phenotypic variation across lineage radiations. However, while wide geographic range and high phenotypic variability have previously been linked to longer lineage durations (Liow Reference Liow2007; Payne and Finnegan Reference Payne and Finnegan2007), drawing causative links between these variables has proved challenging (Foote et al. Reference Foote, Crampton, Beu and Cooper2008). It is therefore unclear whether B. rhombiferus's lineage persistence can be explained by its high morphological variability and/or wide geographic range, or vice versa. A stronger understanding of the links between geographic range and morphological variability is also needed. While all three variables are highly conflated, in the clades examined here, incipient species form as subsets of the geographic range and stock of variation present in the ancestor. Future work will be needed to better explain the links between morphological variation, geographic range, and lineage duration in Barycrinus and other lineages.

Budding, Phylogenetic Pattern, and Paleobiological Process

A pattern of multiple descendants arising from a single, long-lived, ancestor was uncovered in both Ectocion and botryocrinids. Such complex relationships cannot be represented meaningfully in a purely bifurcating cladogram, resulting only in the appearance of “rogue” taxa and polytomies. This shortcoming of using cladograms as a proxy of evolutionary relationships in paleobiology has long been recognized (e.g., Wagner and Erwin Reference Wagner, Erwin and Anstey1995; Bapst Reference Bapst2013). Biological reality demands the accommodation of diverse speciation modes when reconstructing phylogeny in the fossil record. Moving forward, it is important to consider how diverse biological processes such as multiple buddings, anagenesis, and even hybridization (Ausich and Meyer Reference Ausich and Meyer1994) might shape relationships among fossil lineages. Although substantial advances have been made recently in the evaluation and representation of a greater diversity of speciation modes (Bapst and Hopkins Reference Bapst and Hopkins2017; Stadler et al. Reference Stadler, Gavryushkina, Warnock, Drummond and Heath2018; Parins-Fukuchi et al. Reference Parins-Fukuchi, Greiner, MacLatchy and Fisher2019; Wright et al. Reference Wright, Wagner and Wright2021, Reference Wright, Bapst, Barido-Sottani and Warnock2022), many of these still operate from the premise that most relationships tend to be bifurcating and that hypothetical ancestors predominately link fossil lineages. This is largely a matter of implementation, stemming from the fact that most advances in phylogenetic tree searching over the past several decades have focused on inferring trees between contemporaneous lineages and perhaps also the pattern cladists’ denial of the identifiability of ancestral taxa (Engelmann and Wiley Reference Engelmann and Wiley1977). In the absence of overturning information (which may also exist), it is simply more parsimonious to initially assume hypotheses of direct ancestry, because these do not demand the ad hoc construction of unobserved “ghost” lineages to explain phylogeny (Polly Reference Polly1997). As a result, paleobiology might benefit from algorithms that begin from the premise that taxa originating at different times represent ancestor–descendent sequences a priori and allow character data to overturn this starting assumption when necessary.

Gahn and Kammer (Reference Gahn and Kammer2002) provided an excellent example of how a cladistic analysis might be supplemented with extensive natural history knowledge to derive deep evolutionary insights. While developing a thorough understanding of the full context and nuances of specimen-based data forms the foundation for sound paleobiological research, such insights can be supported by quantitative evidence and thorough graphical explorations. Once biological patterns can be reconstructed with a reasonably high degree of confidence, it becomes possible to narrow interpretations into a smaller range of possible explanatory, process-driven, scenarios (Fisher Reference Fisher1981). Evidence supporting alternative scenarios consistent with the reconstructed pattern might then be weighed using statistical criteria. Nevertheless, the first step is to further develop theory and methods supporting the reconstruction of ancestor–descendant relationships. While much important work has already been done in this area (see references cited in “Material and Methods”), the results here especially highlight the importance of a continued rethinking of paleobiological phylogenetics and encourage a further untethering of the field from the shackles of cladistic dogma.

Ancestral Polymorphism, Parallel Speciation, and Adaptive Radiation

A major issue in the biology of adaptive radiation has been understanding how ecology shapes the phenotypes displayed by incipient species in the process and aftermath of adaptive radiation. Several authors have highlighted the role of parallel evolution in shaping these episodes (Schluter and Nagel Reference Schluter and Nagel1995). Under this scenario, rapidly forming species evolve similar traits as they radiate into similar ecological niches. This model of adaptive radiation has been thought to be incompatible with the classic model of peripatric speciation (Mayr Reference Mayr1963), wherein species form rapidly during founder events. Paleobiologists might be inclined to liken these scenarios to budding speciation. The incompatibility between these two models presumably stems from the small population sizes displayed by the descendants that result from budding speciation, which would decrease the efficiency with which natural selection within each new population fixes similar variants in parallel among newly formed species.

While many examples of parallel speciation exist in the neontological literature, the paleobiological literature remains rife with examples of budding, suggesting a role for peripatry in the formation of new lineages. Careful examination of how variation is filtered and maintained at different taxonomic levels across varying ecological contexts might provide the key to reconciliation between these apparently conflicting views. Adaptation that occurs when populations move into new habitats can be fueled by large pools of standing ancestral variation (e.g., McGee et al. Reference McGee, Borstein, Meier, Marques, Mwaiko, Taabu and Kishe2020). If selection is strong enough among the descendant lineages, advantageous alleles may still overcome the effects of drift in small, peripherally isolated populations, allowing ancestral variation to fix in beneficial ways (Fig. 3B). This demands that the ancestral and descendant lineages exist in distinct ecological conditions, because the maintenance of variation in the ancestral population would require a different, balancing, selective regime than the positively selective descendants. This type of dynamic may be shown between large, marine, ancestral populations of sticklebacks and their smaller descendant freshwater populations (e.g., Schluter and Conte Reference Schluter and Conte2009). Species selection also may be able to generate a similar pattern when the effect of drift is too great for selection to operate at the population level. Variation in peripherally isolated populations might become fixed randomly, with only populations that stochastically fixed beneficial alleles able to persist. The Barycrinus analyses here are more consistent with the latter scenario, which showed that the pattern of character state sorting in a descendant lineage cannot be distinguished from drift. Each of these alternatives would yield similar patterns to parallel speciation, with the only difference being the level at which variation filters out deleterious variation. While population-level positive selection may have driven the appearance of parallel speciation in sticklebacks, the Barycrinus analysis illustrates the possible role for species selection in generating similar patterns by differentially culling descendant lineages that each inherited a random suite of characters from its ancestor.

Long-Term Maintenance of Polymorphisms

The trans-specific maintenance of polymorphic characters creates a natural link between the population processes maintaining phenotypic and genetic variation and the macroevolutionary processes shaping the evolution of lineages. Each of the datasets examined here displays polymorphisms maintained over long timescales, both within and between species. The polymorphisms present within lineages were confirmed or implied by the original studies to have been present throughout the duration of each lineage, even though trait frequencies may have oscillated over time in some cases. The true temporal persistence of these polymorphisms was also supported by their frequent appearance across species boundaries. While polymorphisms often sorted into monomorphic descendant lineages, they also persisted in several cases, such as the transition from E. mediotuber to E. osbornianus or B. rhombiferus and B. spurius. Patterns in the maintenance and sorting of polymorphic traits across species boundaries in Barycrinus highlight how variation at the population level stochastically generates variation between species. The transformation of intrapopulation into trans-specific variation paves the way for higher-level processes, such as species selection (Stanley Reference Stanley1975), to operate. Because evolution is fundamentally rooted in the study of biological variation, it makes sense that understanding its persistence across scales provides the indispensable link between population processes and paleobiological patterns. Further developing this framework may provide the key to developing a true understanding of macroevolutionary process and how it connects to the mechanisms of population genetics.

Linking Population and Macroevolutionary Processes

When maintained over long periods against a consistent backdrop of balancing selection, lineages that maintain polymorphic variation will be better suited to persist compared with lineages that lose diversity to drift. It has been argued that the basic prerequisite for selection to operate above the species level is that phenotypic variation be fixed within lineages but variable between lineages (Stearns Reference Stearns, Raup and Jablonski1986). However, the persistence of polymorphisms maintained over long periods within and distributed between fossil lineages adds further complexity. When balancing selection is the maintaining force, even lineages that display variation may be subject to species selection under certain conditions. These polymorphic lineages display what might be viewed as a lineage-level analogue to heterozygote advantage (Fig. 4, left). Under this scenario, bet-hedging in the face of spatial or temporal variation in environment and/or NFDS at the population level maintains stability in trait or genotype frequencies that facilitates higher-level dynamics, such as species selection, to operate simultaneously. In this case, the necessary condition for species selection to operate would be ecologically induced maintenance of polymorphism (potentially both within and across lineages), rather than a total lack of intraspecific variation. On the other hand, lineages that fix variation from polymorphic ancestors may achieve greater persistence by escaping into a new ecological niche that does not impose balancing selection (Fig. 4). Overall, it is important to consider both inter- and intraspecific variation and the ecological contexts within which they are maintained and sorted among lineages when exploring higher-level evolutionary dynamics.

Figure 4. Species selection dynamics stemming from a persistently polymorphic ancestral population. In this hypothetical scenario, negative frequency-dependent selection forms the selective background in the ancestor. When descendant lineages randomly fix this ancestral variation as they originate, they demonstrate low survivorship in the ancestral niche. Only lineages that can escape and radiate into a new niche while fixing ancestral variation display high survivorship. Ecological opportunity afforded by the new niche may even facilitate enhanced lineage survivorship and proliferation if the trait fixed in the descendant is congruent with the selective demands of the new habitat.

While the level at which variation is displayed remains a critical point in identifying the boundary conditions under which higher-level selection can operate, perhaps an even more crucial point lies in considering the selective and ecological contexts occupied by different lineages. Rather than demanding the absence of variation within species, the conditions allowing species-level selection may instead be specified by comparing the distribution of variation within species (poly- vs. monomorphic) to the ecological conditions occupied across species (e.g., does competition or predation universally impose frequency-dependent fitness effects within species?). The longer durations exhibited by B. rhombiferus and B. spurius may stem from higher species-level fitness for polymorphic taxa, which could be driven by balancing forces such as environmental variability or negative frequency dependence resulting from competition or predation. If intraspecific polymorphism is maintained by environmental heterogeneity associated with more generalist ecologies, the new niches occupied by successful monomorphic lineages should tend to be more specialized. This would yield distinct macroevolutionary dynamics, with generalist polymorphic lineages displaying high lineage survivorship and specialist monomorphic lineages displaying rapid species turnover. This dynamic would explain the persistence of polymorphism in the fossil record by the ecological dynamics displayed by Mississippian crinoids (Kammer et al. Reference Kammer, Baumiller and Ausich1997). Nevertheless, moving forward, it will also be important to test such hypotheses within the context of geographic range and abundance, which may also impact lineage duration and turnover patterns (Liow Reference Liow2007).

It has long been hypothesized that biased patterns of extinction among new species might shape macroevolutionary patterns observed in the fossil record by culling “ephemeral” species before they are able to fossilize (Raup and Stanley Reference Raup and Stanley1978: p. 105; Stanley Reference Stanley1979; Rosenblum et al. Reference Rosenblum, Sarver, Brown, Des Roches, Hardwick, Hether, Eastman, Pennell and Harmon2012; Rabosky Reference Rabosky2013). Such biased extinction patterns could arise when new lineages are unable to adapt rapidly enough to new environmental conditions (De Lisle et al. Reference De Lisle, Punzalan, Rollinson and Rowe2021). Meanwhile, paleontological work has suggested that high morphological variation within species might help fuel lineage radiations (Webster Reference Webster2007). If drawn from highly diverse ancestral populations, the variation displayed by rapidly radiating descendant lineages will become sorted through a mix of stochasticity and adaptation, potentially occurring at multiple levels. Incipient species that are able to draw upon a deep well of ancestral variation may stand a greater chance of inheriting “rescue” alleles that enable them to escape extinction long enough to avoid nonpreservation in the fossil record due to ephemerality.

The “natural experiments” displayed by descendant Barycrinus species illustrate how filtering of ancestral variation, a process that occurs at the population level, might form the basic conditions and raw material for macroevolutionary processes, such as species selection, to operate. Random sorting of ancestral variation into descendant lineages is a pattern predicted by classic evolutionary theory (e.g., Simpson Reference Simpson1944; Mayr Reference Mayr1963; Wright Reference Wright1982). The manner by which this occurs, when compared against the range of selective conditions inhabited by incipient lineages, might explain how variation at the population level in highly diverse ancestral populations might filter into descendant lineages to shape macroevolutionary dynamics. Recent work has suggested that gene tree discordance, which is at least partially caused by incomplete lineage sorting (ILS)—the random sorting of ancestral variation into descendant lineages—is greater during periods of rapid phenotypic innovation, such as during the early evolution of mammals, birds, or angiosperms (Parins-Fukuchi et al. Reference Parins-Fukuchi, Stull and Smith2021). This link implies high genetic diversity (and thus perhaps high phenotypic variation as well) within lineages during the early stages of rapid clade diversification. Such variation will stand a good chance of sorting in ways that are discordant with the order of species divergences, yielding two main effects: (1) high gene-tree discordance and (2) the seeming appearance of rapid morphological variation distributed haphazardly across lineages. The resulting combination of stochastic sorting, parallel speciation, and species selection may yield the extensive gene-tree discordance and hemiplasy (Avise et al. Reference Avise and Robinson2008; Gurrero and Hahn Reference Guerrero and Hahn2018) that often accompany rapid radiations. Future work drawing more explicit links between coalescent expectations under ILS and the sorting of phenotypic ancestral variation across fossil lineages may help shed light on how population processes provide the fuel for large-scale macroevolutionary processes and patterns to operate.