Speciation by selection: A framework for understanding ecology’s role in speciation

Abstract

Abstract Speciation research during the last several decades has confirmed that natural selection frequently drives the generation of new species. But how does this process generally unfold in nature? We argue that answering this question requires a clearer conceptual framework for understanding selection’s role in speciation. We present a unified framework of speciation, providing mechanistic descriptions of fundamentally distinct routes to speciation, and how these may interact during lineage splitting. Two major categories are recognized: reproductive isolation resulting from (1) responses to selection, “speciation by selection,” or (2) non-selective processes, “speciation without selection.” Speciation by selection can occur via three mechanisms: (1) similar selection, (2) divergent selection, and (3) reinforcement selection. Understanding ecology’s role in speciation requires uncovering how these three mechanisms contribute to reproductive isolation, and their relative importance compared to non-selective processes, because all three mechanisms can occur side-by-side during speciation. To accomplish this, we highlight examination of groups of organisms inhabiting replicated environmental gradients. This scenario is common in nature, and a large literature illustrates that both parallel and non-parallel responses to similar environments are widespread, and each can result in speciation. This recognition reveals four general pathways of speciation by similar or divergent selection—parallel and nonparallel responses to similar and divergent selection. Altogether, we present a more precise framework for speciation research, draw attention to some under-recognized features of speciation, emphasize the multidimensionality of speciation, reveal limitations of some previous tests and descriptions of speciation mechanisms, and point to a number of directions for future investigation.