Speciation and Evolutionary Divergence

Introduction

One of the key objectives of evolutionary biology is to explain the different modes of divergence and speciation that foster biological diversity. Speciation refers to an evolutionary process that often culminates in the formation of new entities, which may be referred to as species; that is, groups of organisms that are mostly reproductive isolated (Mayr, 1942, Price, 2008). This process has historically been categorized into three main modes: sympatric, parapatric, and allopatric, each based on spatial relationships between distinct populations (Fitzpatrick et al., 2008). Classical allopatric speciation is the divergence of populations that are geographically separated from each other without movement of individuals between them (Mayr, 1942, Gavrilets, 2003, Gavrilets, 2004, Coyne and Orr, 2004, Fitzpatrick et al., 2008, Price, 2008 ). Sympathetic speciation involves the evolution of reproductive isolation while population ranges overlap (Coyne and Orr, 2004). Parapatric speciation is the origin of new species in which gene flow occurs across a spatially restricted contact zone such that only a fraction of each population has a high probability of emigration or interaction with immigrants (Smith, 1955, Endler, 1977, Futuyma and Mayer, 1980, Fitzpatrick et al. ., 2008). These geographic modes of speciation can be thought of as existing on a continuum, on which allopatric and sympatric speciation represent endpoints of varying amounts of gene flow (from zero to maximum), while parapatric speciation occupies a space representing intermediate gene flow between these extremes (Butlin et al., 2008). ). ). , Gavrilets, 2014).

The study of speciation has often focused on these geographic modes of divergence. There is considerable debate about whether allopatric speciation is prevalent (e.g. Coyne and Orr, 2004), whether sympatric speciation is possible and, if so, how often it may occur (e.g. Berlocher and Feder, 2002, Bolnick and Fitzpatrick, 2007 ). . In some cases, geographic isolation alone has been shown to lead to divergence when isolated populations live in allopatry. For example, allopatric speciation is common in molluscs (78% of species pairs), partly due to their low dispersal rates (Hernández-Hernández et al., 2021). Similarly, among terrestrial gastropods living in island archipelagos, allopatric species pairs predominate (96%), with most species endemic to a single island (Holland and Cowie, 2009, Rundell, 2008, Jordaens et al., 2009, Hernández and Hernández et al., 2021).
Although the geographic distribution of populations is important for understanding speciation, other factors such as ecological, environmental and behavioral differences between populations are increasingly recognized as important drivers of population divergence and speciation (Schluter, 2001, McKinnon et al., 2004, Ruegg et al. al., 2012, Verzijden et al., 2012, Withrow et al., 2014). Although these factors can operate within each category of geographically driven modes of speciation (allopatric, parapatric, and sympatric; Gavrilets, 2003), their presence is particularly important in enabling the development of parapatric or sympatric speciation (speciation with gene flow; Rundle and Nosil, 2005, Nosil , 2008, Feder et al., 2012). For example, ecological and sexual selection are considered major evolutionary forces that often drive insect speciation (Arnqvist et al., 2000, Forbes et al., 2017, Hernández-Hernández et al., 2021), and spatial relationships may be less important. An example of ecological divergence occurs in the Timema insect, where ecotypes live on different host plants (Nosil et al., 2008), in which populations adapting to contrasting environments develop greater reproductive isolation than populations adapting to similar environments (Rice and Hostert, 1993, Schluter and Nagel, 1995, Schluter, 2009). Environmental factors are also often an important driver of divergence (Hernández-Hernández et al., 2021), and this occurs in many vertebrate groups, including salamanders (Kozak and Wiens, 2010), frogs (Moen and Wiens, 2017), birds ( Cooney et al., 2016) and mammals (Castro-Insua et al., 2018). Finally, behavior is commonly implicated in prezygotic isolation barriers, including ecological and behavioral differences between species (Hernandez-Hernandez et al., 2021). For example, species-specific vocalization and communication are often important reproductive isolation mechanisms in birds and frogs (e.g., Edwards et al., 2005, Hoskin et al., 2005, Boul et al., 2007, Uy et al., 2018).

In birds, allopatric speciation has historically been considered the main route to speciation (Mayr, 1963, Coyne and Orr, 2004, Price, 2008). However, genomic data increasingly identify groups that do not fit this model and instead suggest that speciation has progressed with at least some gene flow (Mallet et al., 2016, Morales et al., 2017, Penalba et al., 2019, Rheindt et al. . .Edwards et al., 2011, Zarza et al., 2016, McLaughlin et al., 2020, Winker, 2021). One example of how the allopatric speciation model is not ideal for speciation in birds is that many long-distance, seasonally migratory birds often exhibit semiannual transcontinental and transoceanic movements that may prevent different populations from experiencing long periods of strict allopatry (Winker, 2010). , Peters et al., 2012 ), increasing the likelihood of divergence with gene flow.