More adventures in Speciation

As Andrew’s last post demonstrates, uncovering the primary mechanisms of speciation - barriers to gene exchange between populations - remains a topic of active debate, even among the most eminent researchers in the field. Part of this debate potentially, and perhaps paradoxically, is a result of the fact that the field was dominated by conceptual and theoretical contributions until the last decade which has seen an explosion of empirical research. The main conceptual mechanisms of speciation, measured as the accumulation of reproductive isolation, are rooted in sexual selection, ecological differences (i.e. natural selection) and physical isolation. Data from different systems often fit nicely into one of these three umbrellas, lending support to the original theories, but leave us scratching our heads to understand which mechanism(s) are THE main drivers of the process. Our latest paper,recently published in PLoS ONE (http://dx.plos.org/10.1371/journal.pone.0015659) suggests that rather than looking for a single winner, the answer may become clearer by closer integration. In collaboration with researchers from the University of Maine and Dalhousie University, we examined patterns of female mate choice and male mating success in Trinidadian guppies from nine populations in 4 different rivers.

Avid readers of this blog or anyone who has picked up a biology textbook, will be familiar with the guppies, as they are one of the few model organisms for studying adaptation in the wild. The guppy’s small size, agility, and freakishly high fecundity allowed it to colonize upstream sections of rivers above large waterfalls, unlike its larger, predatory neighbours. This sets the stage for a natural laboratory for observation and experimentation as upstream guppies have escaped to guppy heaven, banishing their cousins to the hell of a life of high mortality risks. But of course, what doesn’t kill you makes you stronger, and high-predation guppies have indeed adapted to their lives in hell allowing them to escape quickly, mature early, hide well, and limit their sexual colouration to remain as inconspicuous as possible. Their cousins above are not so careful or visually discreet. Males in particular are generally more colourful, possibly because females generally prefer to mate with colourful males. When these guys move or get flushed downstream, we know they suffer the consequences with reduced survival.

Since ecological and physical isolation has led to adaptive differences in multiple traits, one of which is a target of both mate choice and survival, the stage is set for speciation as far as has been documented in similar systems. Yet, evidence for reproductive isolation between guppy populations has so far been sparse and inconsistent. What we found is that while low-predation females consistently discriminate against high-predation males (regardless of their river of origin), high-predation females only discriminate against low-predation males from upstream in their own rivers. This pattern is not only consistent in lab tests from paired populations in three different rivers, but also evident in the field experiments. Here, we set up enclosures in a high-predation stream and allowed resident males and two populations of low-predation males (one neighbour population and another further away) to compete for fertilizations with resident virgin females. Paternity analyses revealed that high-predation males only substantially outcompete the neighbouring low-predation males. Together, this study shows evidence for mating isolation in guppies but this isolation is likely driven by more than one mechanism: for females in high-predation environments, it’s selection against maladapted low-predation migrant males (reinforcement), whereas for low-predation females it’s selection against particular traits related to survival in high-predation. What these traits are specifically, how they influence mating success, and how preferences are evolving and respond to selection remain open questions and important areas for future research.

So although the latest chapter in the guppy story doesn’t necessarily fall into textbook expectations, it nonetheless shows the strength in not only looking for evidence of speciation where it’s most likely to be found, but by focusing on situations where it isn’t apparent we may be able to start to untangle the ecological limits to evolutionary differentiation and the evolutionary limits to ecological differentiation.