The Evolution of Female Mating Preferences: Differentiation From Species With Promiscuous Males Can Promote Speciation

Abstract

Abstract. Females of many species are frequently courted by promiscuous males of their own and other closely related species. Such mating interactions may impose strong selection on female mating preferences to favor trait values in conspecific males that allow females to discriminate them from their heterospecific rivals. We explore the consequences of such selection in models of the evolution of female mating preferences when females must interact with heterospecific males from which they are completely postreproductively isolated. Specifically, we allow the values of both the most preferred male trait and the tolerance of females for males that deviate from this most preferred trait to evolve. Also, we consider situations in which females base their mating decisions on multiple male traits and must interact with males of multiple species. Females will rapidly differentiate in preference when they sometimes mistake heterospecific males for suitable mates, and the differentiation of female preference will select for conspecific male traits to differentiate as well. In most circumstances, this differentiation continues indefinitely, but slows substantially once females are differentiated enough to make mistakes rare. Populations of females with broader preference functions (i.e., broader tolerance for males with trait values that deviate from females' most preferred values) will evolve further to differentiate if the shape of the function cannot evolve. Also, the magnitude of separation that evolves is larger and achieved faster when conspecific males have lower relative abundance. The direction of differentiation is also very sensitive to initial conditions if females base their mate choices on multiple male traits. We discuss how these selection pressures on female mate choice may lead to speciation by generating differentiation among populations of a progenitor species that experiences different assemblages of heterospecifics. Opportunities for differentiation increase as the number of traits involved in mate choice increase and as the number of species involved increases. We suggest that this mode of speciation may have been particularly prevalent in response to the cycles of climatic change throughout the Quaternary that forced the assembly and disassembly of entire communities on a continentwide basis.

Reinforcement generates reproductive isolation between neighbouring conspecific populations of spadefoot toads

“…We also found that females from mixed-and pure-species populations express divergent preferences for conspecific male call characters. These divergent preferences are likely to be the result of reinforcement, because the evolution of enhanced discrimination of conspecifics from heterospecifics will often concomitantly affect patterns of mate choice among conspecifics [1,8,10,22,57]. That mixed-and pure-species populations exhibit such divergent preferences is significant, because it indicates that female preferences can become locally adapted to the presence of heterospecifics, even at a relatively fine spatial scale.…”

“…When interactions with heterospecifics are costly (as when hybridization results in offspring of low fitness), selection should favour behaviours that prevent reproductive interactions, thereby enhancing isolation between species (or incipient species) to the point where gene exchange between them is reduced or completely eliminated [3,36,38,39]. Yet reinforcement (and, more generally, reproductive character displacement) may also serve to initiate divergence-and possibly speciation [1,2,[6][7][8][9][10][11][12][13][14][15][16][17]43]. Indeed, if reinforcement occurs with different heterospecifics in different parts of a focal species's range, or in different ways across sympatry and allopatry, it can contribute to 'speciation cascades' in which multiple speciation events are triggered by reinforcement [1,8,13], a process that has also been called the 'cascade reinforcement hypothesis' and 'RCD speciation' [9,15,16,20] (see also [6]).…”

“…If such trait differences become sufficiently pronounced, individuals in sympatry or allopatry may fail to recognize members of the alternative population type as acceptable mates [8,11,12,17]. Conspecific populations in sympatry and allopatry could thereby become reproductively isolated, and, ultimately, speciation between them could occur [1,2,[6][7][8][9][10][11][12][13][14][15][16][17] (but see [18,19]). …”

“…Second, whether character displacement drives divergence between allopatry and sympatry depends on its effect on mating behaviour [1,2,[7][8][9][10]13,21,22]. Generally, reproductive character displacement is expected to promote the evolution of female mate preferences that minimize interactions with heterospecifics.…”

Sex differences in developmental plasticity and canalization shape population divergence in mate preferences

“…These features of the ecology and natural history of demoiselles make them excellent study organisms to investigate how sex differences in developmental plasticity and learning might affect local adaptation and population divergence in the presence or absence of conspecifics and in the face of gene flow. As these demoiselles and other odonates (dragonflies and damselflies) often show weak ecological differentiation between species [25,26], they challenge models of ecological speciation and point to non-ecological speciation mechanisms through social selection, sexual selection, sexual conflict and/or learning [27][28][29][30].…”