Population fragmentation drives up genetic diversity in signals of individual identity

Abstract

Many species advertise their unique identity to conspecifics using dedicated individuality signals: one familiar example is human faces. But how unique in the global population do these signals need to be? While human faces are highly variable, each person interacts with many fewer individuals than are found in the total population. This raises the question of how evolutionary mechanisms drive up population‐wide diversity when selection occurs at such a local level. We use an individual‐based model in which individuals broadcast their identity and quality in separate, genetically‐coded signals. Mimicking, for example, scent marking mammal species, females in the model assess males using the quality signal, then attempt to relocate the highest quality male using his identity signal. We ask how population fragmentation affects genetic diversity in the individual identity‐signalling region under sexual selection, predicting one of two opposing outcomes: 1) divided populations evolve fewer signal variants globally, since repetition of signals is not costly when individuals interact only with local conspecifics, or 2) stochasticity in mutation and selection cause divergence among subpopulations, increasing the global number of signal variants. We show that local selection drives up global genetic diversity substantially in fragmented populations, even with extremely low rates of dispersal. Because new signal variants arise by mutation and then sweep through their subpopulation, a fragmented population has more global signal variation. This result furthers our understanding of how high levels of diversity in individuality signals are maintained.

Coevolution of cognitive abilities and identity signals in individual recognition systems

“…With respect to individual recognition, the evolutionary dynamics of sender and receiver traits may provide insights into the processes shaping signal diversity and cognition, respectively. Previous models examining the evolution of sender phenotypes used for recognition have examined the extent of diversity expected within a population in relation to various scenarios dealing with competition or choice [2,14,15,22,23]. These models have not considered, however, the dynamic interplay of sender phenotypic diversity with receiver cognition.…”

Strong spatial population structure shapes the temporal coevolutionary dynamics of costly female preference and male display

“…Our work further emphasises the need to consider sexual selection in a spatially explicit ecological context to understand the evolution and persistence of sexual traits (Payne and Krakauer 1997; Day 2000; M’Gonigle et al 2012). A recent study examined effects of population fragmentation on the diversity of individual identity signals under sexual selection, and found that global signal diversity increased by 10-15% in fragmented versus unfragmented habitat (Dytham and Thom 2020). Our results similarly suggest that fragmentation (here represented by strong spatial structure) elevates genetic variation in male sexual signals and extensively prolongs the persistence of costly female preference.…”

“…Costly female preferences for local male displays could then be maintained by recurring immigration (Day 2000; Proulx 2001; Reinhold 2004). This mechanism could be commonplace if mating preferences and resulting sexual selection vary spatially (Payne and Krakauer 1997; Day 2000; Brooks 2002; Kingston et al 2003; Chunco et al 2007; Gray and McKinnon 2007; M’Gonigle et al 2012; Wellenreuther et al 2014; Ponkshe and Endler 2018; Dytham and Thom 2020). Indeed, several models have shown that evolution of divergent female preferences can cause spatially variable sexual selection, for example given spatially varying natural selection on male display (Lande 1982; Day 2000), varying male dispersal depending on mating success (Payne and Krakauer 1997) and spatial variation in carrying capacity combined with mate-search costs in females (M’Gonigle et al 2012).…”

“…Therefore, the potential consequences of limited gene flow in facilitating persistence of V a underlying display and associated preference evolution over long biological timeframes remain largely unexplored. Yet, within spatially structured populations, gene flow and genetic drift are both prominent processes which could shape G-matrices of sexual traits (Guillaume and Whitlock 2007; Dytham and Thom 2020; Reid and Arcese 2020), and thereby modulate costly preference and display coevolution.…”

“…Yet, within spatially structured populations, gene flow and genetic drift are both prominent processes which could shape G-matrices of sexual traits (Guillaume and Whitlock 2007;Dytham and Thom 2020;Reid and Arcese 2020), and thereby modulate costly preference and display coevolution. Furthermore, although sexual selection is predicted to cause male display phenotypes to diverge from naturally selected optima (Lande 1981), the population dynamic consequences of resulting increased male mortality are seldom explicitly considered (Tanaka 1996;Kokko and Brooks 2003;Martínez-Ruiz and Knell 2017).…”