Persistent postmating, prezygotic reproductive isolation between populations

Abstract

Studying reproductive barriers between populations of the same species is critical to understand how speciation may proceed. Growing evidence suggests postmating, prezygotic (PMPZ) reproductive barriers play an important role in the evolution of early taxonomic divergence. However, the contribution of PMPZ isolation to speciation is typically studied between species in which barriers that maintain isolation may not be those that contributed to reduced gene flow between populations. Moreover, in internally fertilizing animals, PMPZ isolation is related to male ejaculate—female reproductive tract incompatibilities but few studies have examined how mating history of the sexes can affect the strength of PMPZ isolation and the extent to which PMPZ isolation is repeatable or restricted to particular interacting genotypes. We addressed these outstanding questions using multiple populations of Drosophila montana. We show a recurrent pattern of PMPZ isolation, with flies from one population exhibiting reproductive incompatibility in crosses with all three other populations, while those three populations were fully fertile with each other. Reproductive incompatibility is due to lack of fertilization and is asymmetrical, affecting female fitness more than males. There was no effect of male or female mating history on reproductive incompatibility, indicating that PMPZ isolation persists between populations. We found no evidence of variability in fertilization outcomes attributable to different female × male genotype interactions, and in combination with our other results, suggests that PMPZ isolation is not driven by idiosyncratic genotype × genotype interactions. Our results show PMPZ isolation as a strong, consistent barrier to gene flow early during speciation and suggest several targets of selection known to affect ejaculate‐female reproductive tract interactions within species that may cause this PMPZ isolation.

Strength of sexual and postmating prezygotic barriers varies between sympatric populations with different histories and species abundances

“…In our study, the reasons for decreased egg hatch rate were traced in crosses between D. flavomontana females and D. montana males, and between D. flavomontana flies from different population types, and in both cases failure in egg development appeared to be due to an inability of sperm to enter the egg. Similar barriers have been detected also between other virilis group species (Sweigart 2010;Sagga and Civetta 2011;Ahmed-Braimah and McAllister 2012) and previously between D. montana populations (Jennings et al 2014b;Garlovsky and Snook 2018).…”

“…Similar barriers have been detected also between other virilis group species (Sweigart ; Sagga and Civetta ; Ahmed‐Braimah and McAllister ) and previously between D. montana populations (Jennings et al. ; Garlovsky and Snook ).…”

Within-population sperm competition intensity does not predict asymmetry in conpopulation sperm precedence

“…98 99We have previously described prezygotic reproductive isolation between three populations of 100 Drosophila montana, from Crested Butte, Colorado, USA (referred to as Colorado), Oulanka, Finland, 101 and Vancouver, Canada (Fig. S1) [33][34][35][36][37]. All three populations show premating and PMPZ isolation 102 ( Fig.…”

“…Vancouver females discriminate against Colorado 106 males and both populations show non-competitive PMPZ isolation, where females successfully store 107 sperm from foreign males after mating but lay many unfertilised eggs. PMPZ isolation is strongest 108 when Colorado females mate with Vancouver males [35,36]. 109 110 Using the D. montana system, we set out to ask (1) what is the relative timescale of divergence and 111 what role has gene flow played during divergence, (2) do populations show conpopulation sperm 112 precedence (CpSP) and if so, is it concordant with non-competitive PMPZ isolation, (3) is the strength 113 of PMPZ isolation predicted by the strength of postcopulatory sexual selection acting within 114 populations, and (4) do overlapping foreign and coevolved ejaculates interact to alter PMPZ 115 outcomes?…”

The effects of heterospecific mating frequency on the strength of cryptic reproductive barriers

“…These cryptic reproductive barriers have been well-studied in laboratory crosses in which females are mated with single males (i.e. noncompetitive barriers, Ahmed-Braimah & McAllister, 2012;Garlovsky & Snook, 2018;Jennings, Snook, & Hoikkala, 2014;Larson, Hume, Andrés, & Harrison, 2012;Peterson et al, 2011;Poikela et al, 2019;Turissini, McGirr, Patel, David, & Matute, 2017) or to equal proportions of conspecific and heterospecific males (i.e. conspecific sperm precedence or CSP, Bella, Butlin, Ferris, & Hewitt, 1992;Chang, 2004;Davis & Moyle, 2017;Gregory & Howard, 1994;Manier et al, 2013;Peterson et al, 2011;Price, 1997;Price, Kim, Posluszny, & Coyne, 2000;Rose, Brand, & Wilkinson, 2013;Tyler et al, 2013).…”