Detecting Macroevolutionary Self-Destruction from Phylogenies

—Phylogenetic analyses have lent support to the concept of lineage selection: that biological lineages can have heritable traits that influence their capacity to persist and diversify, and thereby affect their representation in biodiversity. While many discussions have focused on “positive” lineage selection, where stably heritable properties of lineages enhance their diversification rate, there are also intriguing examples that seem to represent “negative” lineage selection, where traits reduce the likelihood that a lineage will persist or speciate. In this article, we test whether a particular pattern of negative lineage selection is detectable from the distributions of the trait on a phylogeny. “Self-destructive” traits are those that arise often but then disappear again because they confer either a raised extinction rate or they are prone to a high rate of trait loss. For such a trait, the reconstructed origins will tend to be dispersed across the tips of the phylogeny, rather than defining large clades of related lineages that all share the trait. We examine the utility of four possible measures of “tippiness” as potential indicators of macroevolutionary self-destruction, applying them to phylogenies on which trait evolution has been simulated under different combinations of parameters for speciation, extinction, trait gain, and trait loss. We use an efficient simulation approach that starts with the required number of tips with and without the trait and uses a model to work “backwards” to construct different possible trees that result in that set of tips. We then apply these methods to a number of case studies: salt tolerance in grasses, color polymorphism in birds of prey, and selfing in nightshades. We find that the relative age of species, measured from tip length, can indicate a reduced speciation rate but does not identify traits that increase the extinction rate or the trait loss rate. We show that it is possible to detect cases of macroevolutionary self-destruction by considering the number of tips with the trait that arise from each inferred origin, and the degree to which the trait is scattered across the phylogeny. These metrics, and the methods we present, may be useful for testing macroevolutionary hypotheses from phylogenetic patterns. [Dead-end; diversification; extinction; lineage selection; macroevolution; speciation. ] Phylogenies are increasingly being used to uncover macroevolutionary patterns, particularly through the identification of correlates of diversification rates. Identification of properties of lineages that can be stably inherited by descendant lineages and can increase lineage survival (by reducing extinction rate) or fecundity (by increasing speciation rate) has led to the revival of the concept of “species selection” (Stanley 1979; Williams 1992; Jablonski 2008; Rabosky and McCune 2010). Much of the focus has been directed at “positive” lineage selection, identifying traits that confer a higher diversification rate. But lineages might also be considered to be subject to “negative” selection, if certain stably inherited characteristics lead to a reduction in the likelihood of a lineage with that trait persisting or speciating, such that lineages with those characteristics will decline in representation. In this article, our focus is on a particular form of negative lineage selection, which we will refer to as macroevolutionary self-destruction. This refers to lineage traits that evolve often but cause their own disappearance, either because they are rapidly lost again, or because they raise the extinction rate of the lineage. Asexuality is a classic example of a self-destructive trait that evolves often but does not tend to persist over long evolutionary timescales. Williams (1975) stated that sexually reproductive vertebrates were maladapted, in the sense that they would be rapidly replaced by an asexual variant if it arose, however any such lineage would commit “phylogenetic suicide”, keeping the frequency of asexual species low even in the face of frequent transitions to asexuality. Traits that reduce a lineage’s chance of persisting or diversifying are sometimes referred to as “evolutionary dead-ends”. However, the term “evolutionary deadend” has been used in many different ways to describe a range of macroevolutionary phenomena, for example traits with a short-term advantage but increased chance of extinction (Schwander and Crespi 2009; Pruitt 2013); traits that cause the extinction of a lineage before it has a chance to speciate (Helanterä et al. 2009); traits that decrease the diversification rate (Agnarsson et al. 2006; Igic and Busch 2013; Cieslak et al. 2014); character transitions that are apparently irreversible (Tripp and Manos 2008; Schneider and Michalik 2011; and lineages with no present-day descendants (Luo 2007). Here, we are specifically interested in traits that arise often but have a consistently negative impact on their own persistence, either by increasing extinction rate or due to high rates of trait reversal, or both. Traits that cause their own disappearance have been examined in experimental systems, particularly those where short-term advantages at the individual level may have long-term disadvantages at the lineage level. For example, the rate of accumulation of deleterious mutations in parthenogenetic populations has been compared with that in closely related sexual populations (Neiman and Schwander 2011). 109 at T he A usalian N aonal U niersity on M arch 9, 2016 http://sysbfordjournals.org/ D ow nladed from 110 SYSTEMATIC BIOLOGY VOL. 65 Similarly, the longevity of social colonies established by individuals with different behavioral traits has been compared to determine which traits increase the rate of colony extinction (Pruitt 2013). Traits that confer short-term gain but long-term pain may arise from conflict between individual advantage and population persistence (Parvinen 2005). Examples of “evolutionary suicide” might include runaway selection on sexual ornamentation or armaments that reduce the survival probability of their carriers (Gyllenberg and Parvinen 2001), or “tragedy of the commons” where selfish behavior of individuals compromises the survival of a population (Rankin et al. 2007; Kokko and Heubel 2011). In contrast to studies that have developed populationbased models or experiments, we take a comparative, phylogenetic approach, asking whether traits with negative macroevolutionary consequences can be detected from their distribution on phylogenies. These two viewpoints—microevolutionary from population studies and macroevolutionary from phylogenies— are complementary. Population-level studies provide a real-time view of processes that are open to both observation and manipulation, but such studies are limited in their taxonomic scope, and cannot evaluate long-term consequences over evolutionary timescales. While phylogenetic studies can be used to identify significant patterns and to test the relative fit of different macroevolutionary models, they may be limited in the extent to which they can reveal mechanism. However, the strengths of phylogenetic studies are their taxonomic scope, looking for similar patterns over many different lineages and traits; the timescale, allowing evaluation of processes that play out over millions of years; and their repeatability, allowing statistical analyses to be applied to detecting general patterns. Using Tippy Phylogenetic Distributions to Identify Self-Destructive Traits We ask whether cases of macroevolutionary selfdestruction can be detected from a “tippy” distribution of a discrete trait on a phylogeny. A tippy distribution describes a trait that is dispersed and shallow on a phylogeny, mapped to many tips (terminal edges that connect each contemporary species in the tree to its nearest relative) but relatively few internal edges. We consider two (non-exclusive) ways in which macroevolutionary self-destruction could result in a tippy pattern. The first is trait lability. Here, we take “labile” to mean “changeable”, such that the trait is gained and lost often (Revell et al. 2008). A trait that is highly labile and reversible could change frequently enough that all current origins are recent, and that the trait is not shared with many close relatives. For lability alone to create a tippy pattern, the trait must have a high rate of reversal (loss of trait) relative to the rate of gain, otherwise the trait will define clades of a range of sizes, rather than being present predominantly on many isolated tips. Of course, not all labile traits may be relevant to an examination of macroevolutionary self-destruction, but some labile traits will fall into this category of macroevolutionary phenomena, for example a trait that arises often because of short-term advantages but is soon lost again due to its long-term costs. The second is extinction rate. A trait that increases the likelihood of extinction might generate a tippy pattern because lineages with this trait would be unlikely to persist for long enough to generate deep clades. Several conditions would be necessary for a “suicidal” trait to generate a tippy distribution by raising the extinction rate. First, the trait must arise often, because a rare trait that causes extinction is unlikely to persist long enough to be observed. Second, the extinction rate must be high relative to the speciation rate, such that a lineage with the trait usually does not give rise to many daughter lineages before succumbing to extinction. Otherwise, it might lead to shallow clades of species with the trait, rather than a tippy pattern. These two causes of self-destructive traits are nonexclusive, in that they may both act simultaneously. They are also not the only possible causes of a tippy pattern of a trait on a phylogeny. A recent environmental change might promote parallel adaptation in many different lineages. For example, Batalha et al. (2011) report