Both Geography and Ecology Contribute to Mating Isolation in Guppies

Abstract

Local adaptation to different environments can promote mating isolation – either as an incidental by-product of trait divergence, or as a result of selection to avoid maladaptive mating. Numerous recent empirical examples point to the common influence of divergent natural selection on speciation based largely on evidence of strong pre-mating isolation between populations from different habitat types. Accumulating evidence for natural selection's influence on speciation is therefore no longer a challenge. The difficulty, rather, is in determining the mechanisms involved in the progress of adaptive divergence to speciation once barriers to gene flow are already present. Here, we present results of both laboratory and field experiments with Trinidadian guppies (Poecilia reticulata) from different environments, who do not show complete reproductive isolation despite adaptive divergence. We investigate patterns of mating isolation between populations that do and do not exchange migrants and show evidence for both by-product and reinforcement mechanisms depending on female ecology. Specifically, low-predation females discriminate against all high-predation males thus implying a by-product mechanism, whereas high-predation females only discriminate against low-predation males from further upstream in the same river, implying selection to avoid maladaptive mating. Our study thus confirms that mechanisms of adaptive speciation are not necessarily mutually exclusive and uncovers the complex ecology-geography interactions that underlie the evolution of mating isolation in nature.

Speciation in Freshwater Fishes

“…Such patterns dominate in riverine environments even in groups like African cichlid fishes (Lamboj 2004), and they point to two important predictions: that reproductive isolation as a consequence of evolution in geographical isolation is slow and that reinforcement upon secondary contact among ecologically similar taxa is rare. This is corroborated by many examples of hybridization in contact zones between sister species (April et al 2013, Bossu & Near 2013 and few examples for reinforcement known in fish, with most known cases associated with divergent ecological adaptation (Gregorio et al 2012, Schwartz et al 2010 rather than secondary contact between ecologically similar "allotaxa." Besides isolation of different drainage systems, geographical speciation in river fish can be triggered by niche conservatism within drainage systems.…”

“…Work on guppies that have diverged in life-history and courtship traits between downstream high-predation turbid water and upstream low-predation clear water regimes within Trinidadian streams suggests that reinforcement selection in this system can strengthen behavioral isolation in the population that receives gene flow (Schwartz et al 2010), but whether these mechanisms cause parapatric speciation rather than just local adaptation has not yet been studied. Work on allopatric mosquitofishes occupying contrasting predation regimes in blue holes in the Bahamas provides evidence for by-product speciation, where divergent natural and sexual selection on body shape between predation regimes has incidentally increased reproductive isolation as a by-product (Langerhans et al 2007, Langerhans & Makowicz 2013.…”

Divergent Selection and Then What Not: The Conundrum of Missing Reproductive Isolation in Misty Lake and Stream Stickleback

“…Or maybe a distinction is needed between potential magic traits that are "trivial" versus "important," depending on just how much they contribute to mating isolation [70]. It is also possible that interactions between divergent natural and divergent sexual selection acting on traits, or selection acting in different directions in males and females, (e.g., [11,15,25]) may have undermined the evolution of PAMC.…”

“…Of particular utility is the availability of many independently derived parapatric population pairs that show various levels of geographical separation, adaptive divergence, and gene flow [31][32][33]. Lake/stream stickleback therefore provide an opportunity to quantify the relative importance and symmetry of multiple potential reproductive barriers during the early stages of divergence [79,80] as well as interactions between ecology and the geographical context in the development of these barriers (e.g., [15,19,88]). This, and studies on other taxa with similar levels of variation and replication, together with tests of PAMC in wild and common garden populations, should take us a step closer to understanding the key features of ecological speciation.…”

“…Some of the strongest support comes from laboratory studies showing that mating is more frequent between individuals from similar environments than between individuals from different environments [4][5][6][7][8][9][10]. However, some recent work suggests that positive assortative mate choice (henceforth PAMC) does not always evolve in response to divergent selection [11][12][13][14][15]. These results suggest the importance of other modifying factors that influence the evolution of PAMC-even when divergent selection and adaptive divergence are present [16,17].…”