Paleobiology, 47(2), 2021, pp. 236–250 DOI: 10.1017/pab.2020.60 Article Geographic contingency, not species sorting, dominates macroevolutionary dynamics in an extinct clade of neogastropods (Volutospina; Volutidae) Dana S. Friend* , Brendan M. Anderson , and Warren D. Allmon Abstract.—Rates of speciation and extinction are often linked to many ecological factors, traits (emergent and nonemergent) such as environmental tolerance, body size, feeding type, and geographic range. Mar- ine gastropods in particular have been used to examine the role of larval dispersal in speciation. However, relatively few studies have been conducted placing larval modes in species-level phylogenetic context. Those that have, have not incorporated fossil data, while landmark macroevolutionary studies on fossil clades have not considered both phylogenetic context and net speciation (speciation–extinction) rates. This study utilizes Eocene volutid Volutospina species from the U.S. Gulf Coastal Plain and the Hampshire Basin, U.K., to explore the relationships among larval mode, geographic range, and duration. Based on the phylogeny of these Volutospina, we calculated speciation and extinction rates in order to compare the macroevolutionary effects of larval mode. Species with planktotrophic larvae had a median duration of 9.7 Myr, which compared significantly to 4.7 Myr for those with non-planktotrophic larvae. Larval mode did not significantly factor into geographic-range size, but U.S. and U.K. species do differ, indicating a locality-specific component to maximum geographic-range size. Non-planktotrophs (NPTs)were absent among the Volutospina species during the Paleocene–early Eocene. The relative proportions of NPTs increased in the early middle Eocene, and the late Eocene was characterized by disappearance of plankto- trophs (PTs). The pattern of observed lineage diversity shows an increasing preponderance of NPTs; how- ever, this is clearly driven by a dramatic extinction of PTs, rather than higher NPT speciation rates during the late Eocene. This study adds nuance to paleontology’s understanding of the macroevolutionary consequences of larval mode. Dana S. Friend and Warren D. Allmon. Paleontological Research Institution, 1259 Trumansburg Road, Ithaca, New York 14850 U.S.A. E-mail: [email protected], [email protected] Brendan M. Anderson. Department of Geosciences, Baylor University, 101 Bagby Avenue, Waco, Texas 76706 U.S.A. E-mail: [email protected] Accepted: 6 December 2020 *Corresponding author. Introduction that have, have not incorporated fossil data, Many ecological factors have been suggested while landmark macroevolutionary studies on as influencing rates of speciation and extinc- fossil clades (Jablonski and Lutz 1983; Jablonski tion, including feeding type (Levinton 1974), 1986; Hansen 1997) have not considered both population size (Boucot 1975), range of environ- phylogenetic context and net speciation (speci- mental tolerance (Jackson 1974), and dispersal ation–extinction) rates (Krug et al. 2015). Traits ability (Lester et al. 2007). Marine gastropods that lead to increasing rates of speciation might in particular have been the subject of much also lead to a proportionally greater increase in study of the role of dispersal in speciation (Han- rates of extinction, resulting in lower net diver- sen 1978; Jablonski 1987; Jablonski and Valen- sification of the clade possessing said trait tine 1990; McKinney 1997; Crampton et al. (Goldberg et al. 2010). 2010). However, relatively few studies have Gastropods are among the many marine been conducted placing larval modes in invertebrates that undergo a two-stage life species-level phylogenetic context (Collin cycle. The adult gastropod body plan typically 2004; Krug et al. 2015; Sang et al. 2019). Those results in restricted mobility relative to the © The Author(s), 2021. Published by Cambridge University Press on behalf of The Paleontological Society. This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited. 0094-8373/21 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.14, on 01 Oct 2021 at 05:34:56, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2020.60 GEOGRAPHIC CONTINGENCY IN VOLUTID MACROEVOLUTION 237 dispersal that occurs while in the larval form. generally predicted to have a geologically short Two larval types (or developmental modes) duration, and lineages are predicted to have are generally recognized in the literature: higher extinction rates (Jablonski and Lutz planktotrophic and non-planktotrophic (Thor- 1983). Depending on the environmental or eco- son 1950; Jablonski and Lutz 1983). Plankto- logical mechanisms driving extinction, however, trophs (PTs) feed on the plankton, meaning either planktotrophy or non-planktotrophy may their dispersal potential is not nutrient limited be selectively advantageous for reasons unre- (Thorson 1950), and the adults produce relatively lated to dispersal potential (Shuto 1974; larger numbers of eggs. Non-planktotrophs Jablonski and Lutz 1980); for example, non- (NPTs) have a higher per-offspring investment, planktotrophy may be favored when regional potentially increasing survival, but produce productivity declines (Sang et al. 2019). fewer eggs (Jablonski and Lutz 1980). NPTs Dispersal ability also affects the rate of speci- include species with both lecithotrophic (plank- ation. Wide dispersal of larvae effectively mixes tonic, but yolk-feeding) and direct-developing genes from disjunct populations, suppressing larvae. Because non-planktotrophic larvae lack genetic divergence required for speciation. This the structures that facilitate feeding within the model hypothesizes, then, that planktotrophic plankton, they are expected to have more lineages have relatively low speciation rates. In restricted dispersal and consequently both contrast, larvae with restricted dispersal ability lower population interconnectivity (potentially form local populations that remain isolated increasing speciation rates) and smaller geo- after the initial colonization, meaning NPT graphic ranges (potentially increasing extinction lineages likely have higher speciation rates. The risk; Jablonski and Lutz 1980). The exact nature end result of this model is that planktotrophic of the relationship between geographic range species have relatively longer durations, lower and speciation is paradoxical (Jablonski 2017), extinction rates, and low speciation rates; while as greater dispersal ability may lead to either species with non-planktotrophic larvae have increased chances of the formation of peripheral relatively shorter durations, higher extinction isolates or higher interpopulation connectivity, rates and higher speciation rates. Alternatively, depressing speciation (Boucot 1975;Stanley planktotrophic lineages may have more oppor- 1986;AllmonandMartin2014). tunities to form peripheral isolates, leading to The consequences of larval ecology in macro- high speciation rates as well. evolutionary processes have long been dis- A primitive planktotrophic larval mode cussed in the paleobiological literature. Jackson characterizes many gastropod clades, as deter- (1974) and Scheltema (1977, 1978, 1979) devel- mined by phylogenetic methods, for example, oped a model to think about the effect of larval Turritellidae (Lieberman et al. 1993; Sang dispersal ability (i.e., larval type) on speciation et al. 2019), Kermia and Pseudodaphnella (Fedo- and extinction rates. In this model, species sov and Puillandre 2012), Conus (Duda and with planktotrophic larvae (and thus the poten- Palumbi 1999), and neogastropods (Hansen tial to disperse over a large geographic area) can 1982). However, while planktotrophic species easily maintain gene flow between populations, usually give rise to non-planktotrophic species, because larvae from outside populations con- the reverse seems to be a rare exception (Reid stantly “replenish” (Zelnik et al. 2015)popula- 1989). Of the groups mentioned, direct devel- tions that are reduced by local disturbances opment has independently arisen at least two (which are not likely to completely extinguish times, and there were no reversals back to a widespread species from its whole geographic planktotrophy. The lack of reversals can be range). These conditions theoretically result in attributed to the inability to redevelop the spe- species with long durations, and lineages display cialized feeding and swimming features that low extinction rates. Species with non-plankto- characterize planktotrophic larvae once they trophic larvae are likely to have more restricted have been lost (e.g., Strathmann 1974, 1978). geographic ranges, and extinction is more likely High rates of irreversible character change can to occur due to local disturbances and randomly result in the accumulation of distantly related fluctuating populations. Consequently, NPTs are NPTs in the fossil record, similar to state- Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.14, on 01 Oct 2021 at 05:34:56, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/pab.2020.60 238 DANA S. FRIEND ET AL. FIGURE 1. Proposed effects of non-planktotrophy on the proportion of planktotrophic (PT)