Immigrant reproductive dysfunction facilitates ecological speciation

Abstract

The distributions of species are not only determined by where they can survive - they must also be able to reproduce. Although immigrant inviability is a well-established concept, the fact that immigrants also need to be able to effectively reproduce in foreign environments has not been fully appreciated in the study of adaptive divergence and speciation. Fertilization and reproduction are sensitive life-history stages that could be detrimentally affected for immigrants in non-native habitats. We propose that "immigrant reproductive dysfunction" is a hitherto overlooked aspect of reproductive isolation caused by natural selection on immigrants. This idea is supported by results from experiments on an externally fertilizing fish (sand goby, Pomatoschistus minutus). Growth and condition of adults were not affected by non-native salinity whereas males spawning as immigrants had lower sperm motility and hatching success than residents. We interpret these results as evidence for local adaptation or acclimation of sperm, and possibly also components of paternal care. The resulting loss in fitness, which we call "immigrant reproductive dysfunction," has the potential to reduce gene flow between populations with locally adapted reproduction, and it may play a role in species distributions and speciation.

Evidence of rapid adaptive trait change to local salinity in the sperm of an invasive fish

“…show an extreme diversity of species and preferred habitats, indicative of fast local adaptation and niche specialization (Near et al, 2013;Svensson et al, 2017;Taylor & Hellberg, 2005;Thacker, 2014;Yamada, Sugiyama, Tamaki, Kawakita, & Kato, 2009). Spatial sorting, which can aid rapid adaptation (Shine, Brown, & Phillips, 2011), is also supported by differences found between invasion fronts and established areas in the species (Brandner, Cerwenka, Schliewen, & Geist, 2013;Thorlacius, Hellström, & Brodin, 2015).…”

Immigrant and extrinsic hybrid inviability contribute to reproductive isolation between lake and river cichlid ecotypes

“…While some reproductive barriers, such as immigrant inviability, have been assessed in multiple systems, the reduced reproductive success of immigrants has only rarely been estimated in experiments that try to mimic natural conditions (Porter and Benkman ; Svensson et al. ).…”

“…The presence and strength of many potential reproductive barriers, such as natural and sexual selection against migrants and hybrids, can only be experimentally evaluated if divergent populations are brought into secondary contact with each other and/or the divergent environment in natural settings, such as in enclosures in the wild or in mesocosms (Hanson et al 2016). While some reproductive barriers, such as immigrant inviability, have been assessed in multiple systems, the reduced reproductive success of immigrants has only rarely been estimated in experiments that try to mimic natural conditions (Porter and Benkman 2017;Svensson et al 2017).…”

A novel sperm adaptation to evolutionary constraints on reproduction: Pre‐ejaculatory sperm activation in the beach spawning capelin (Osmeridae)

“…At ejaculation, sperm motility activates instantly on contact with an appropriate external medium (plain fresh or salt water in most documented cases). A substantial chemical change in the fertilizing environment requires either (i) post‐ejaculated sperm swimming performance to evolve via natural selection so that populations have sperm locally adapted to their environments (this has been demonstrated on a fine scale in the frog Crinia signifera (Byrne, Dunne, Munn, & Silla, 2015), and the sand goby Pomatoschistus minutus (Svensson et al., 2017)), or (ii) individuals to migrate for reproduction. Although diadromous fishes migrate across marine and freshwater habitats (catadromous salt water spawn, fresh water growth; anadromous fresh water spawn, salt water growth), they must return to their natal environment for spawning because typically marine fish sperm activate upon hypertonic shock with sea water (no activation in fresh water), whereas freshwater fish (and amphibian) sperm activate upon hypotonic shock or decrease in specific ions (Alavi & Cosson, 2006; Browne et al., 2015; Cosson, 2010).…”