the salamander E. eschscholtzii spread south from Oregon along both sides of Sierra Nevada mountains that divide coastal and inland California - over millions of years, the populations gradually diverged Ring Species - gene flow connects adjacent populations, but where the ends of the “ring” meet, populations do not hybridize well  hybrid zone

The idea that species could form in the absence of prolonged isolation has been hotly debated for decades Sympatric speciation occurs when two populations become reproductively isolated “within cruising range” of each other For this to occur, assortative mating has to arise despite gene flow, and without relying on genetic drift Scientists have long theorized that disruptive selection on any trait could potentially lead to sympatric speciation, by splitting one population of generalists into two species of specialists Sympatric speciation: divergence without isolation?

Disruptive selection and assortative mating Thoday and Gibson (1962) - started with 4 wild flies that had different # of bristles on their bodies - their offspring had a normal distribution of bristle #’s

Disruptive selection and assortative mating Thoday and Gibson (1962) - started with 4 wild flies that had different # of bristles on their bodies - every generation, took the 8 flies with the most bristles, and the 8 with the least bristles - let them interbreed to form the next generation - after only 12 generations, there were no intermediate flies: all offspring had either lots of bristles (white), or very few bristles (black)

Disruptive selection and assortative mating What occurred? - disruptive selection: individuals with high or low bristle # survived to reproduce; average number = no reproduction (you were selected against) - over time, no hybrid offspring were produced (no flies with intermediate # of bristles) - assortative mating resulted from selection against hybrids: hairy flies only mated with other hairy flies, and hairless with hairless - effectively became different species in 12 generations (reproductively isolated)

Controversy!.. no one could reproduce the results of Thoday and Gibson -- including themselves (got lucky the 1st time?) It was argued that normally, selection and recombination have opposing effects -- - selection: builds up disequilibrium between trait (bristle #) and mating preference for that trait - recombination: removes disequilibrium between a trait and mating preference for that trait In a sexual population, recombination will prevent disruptive selection from promoting assortative mating and speciation Disruptive selection and assortative mating

hairyprefer selection favors linkage disequilibrium hairy between these 2 traits, since that will mates prevent hybrids from forming hairyprefer recombination removes disequilibrium hairy between these 2 traits, as crossing over events will keep on separating them hairless prefer hairless

Rice (1987) and others demonstrated that you could get around this problem if the trait under selection caused assortative mating as a by-product (basically, coincidentally) -i.e., when assortative mating was a correlated character, instead of a separate trait controlled by other genes Example: habitat choice - if individuals mate only in their preferred habitat, then traits controlling habitat choice indirectly control mating preference - recombination can’t tear down this association, since it’s not due to linkage of alleles controlling two different traits Disruptive selection on habitat choice

The best examples of sympatric speciation are cases of host- switching in specialized arthropods such as insects (herbivores or parasites) Following the introduction of a new host plant by agriculture, some individuals of an insect species will switch onto the new host Adults are most likely to encounter other adults that prefer the same host plant -- results in assortative mating If host preference is heritable, their offspring will repeat the pattern -- and a new host race is born Disruptive selection on habitat choice

The best-studied example is the apple maggot fly, Rhagoletis pomonella This species originally used the hawthorn tree as its host plant Following the introduction of apples into the U.S. around 1850, some individuals switched from hawthorns onto apples In only 150 years, hawthorn and apple races became highly genetically differentiated - but, gene flow still occurs at ~ 6% a year, due to adults that are not perfectly loyal to their original host tree Case study: the apple maggot fly

Despite persistent gene flow, the two host races are genetically differentiated and appear destined to speciate Natural selection maintains 94% reproductive isolation, mainly resulting from different fruiting times of the two trees - apples mature 3 weeks earlier than hawthorn fruit - adults of the apple race hatch earlier to take advantage of new apples, and thus do not overlap with most hawthorn flies This represents a case of incipient speciation... Case study: the apple maggot fly

Steps in sympatric speciationResult (1) mate on preferred hostpromotes assortative mating, so decreases gene flow (2) host-specific adaptationsselects against hybrids, so build up over timereinforces assortative mating (3) other adaptations arise complete the speciation that increase pre-zygotic process isolation, like host fidelity and other mating traits Sequence for speciation by host shift

Parasites also host shift Forbes et al. (2009) Science 323: 776 Genetically distinct host races of Rhagoletis flies known from hawthorn (original), apples, snowberries and blueberries Subsequently shown that specialized parasitic wasps that lay eggs in fly larvae also exist as distinct races, one per fly race - fly races hatch in the same order as their fruit matures: blueberry > apples > hawthorn fruit - wasps hatch in same order As 20% of insects may be parasitic wasps, there is huge potential for speciation by host shift on top of speciation by host shift!

Sympatric speciation by natural + sexual selection VanDoorn et al. (2009) Science 326: 1704 A recent modelling study reported that sympatric speciation can evolve when disruptive natural selection on any ecological trait was paired with a connected male display trait, and sexual selection in the form of female preference for the male display - disruptive selection only: population kept average trait value (like beak size) - add sexual selection: population evolved into 2 distinct forms disruptive selection only disruptive + sexual selection

Sympatric speciation by natural + sexual selection simulated males evolved to invest in display, and females evolved to prefer the male display, because display was connected to male’s ability to use either resource extreme

The concept of speciation was introduced by Darwin, in his book On the Origin of Species by Natural Selection Ironically, for most of the 20 th century, little attention was paid to the role of natural selection as a force driving speciation - focus was on geographical isolation and genetic drift New studies have shown that natural selection in different environments can be a much more powerful evolutionary force than isolation + time (i.e., genetic drift) - the debate is now shifting from allopatry vs. sympatry to ecological speciation (due to natural selection) vs. drift New paradigm: Ecological speciation

Schluter and colleagues have studied stickleback fish in post- glacial freshwater lakes - receding glaciers left behind young lakes initially lacking fish - marine ancestors of the stickleback colonized many such lakes, independently but in parallel - their descendants diversified into 2 forms in each of 6 lakes: (1) limnetic, a small and sleek form that hunts in mid-water (2) benthic, which is larger and hangs out on the bottom Case study: 3-spined sticklebacks

Ecological differences result in size differences: - benthic fish are big + slow; hunt invertebrates on bottom - limnetic fish are smaller, streamlined hunters of plankton Parallel speciation in 3-spined sticklebacks marine ancestor limnetic benthic

In mating trials, benthic fish mated with other benthic fish; limnetic fish mated with other limnetic fish Similar fish mated, no matter which lakes they came from in other words, regardless of genetic similarity – fish from different lakes are not related Parallel speciation in 3-spined sticklebacks Rundle et al. 2000

In mating trials, benthic fish mated with other benthic fish; limnetic fish mated with other limnetic fish Parallel speciation in 3-spined sticklebacks Benthic x limnetic didn’t produce many successful matings

Size-assortative mating  r eproductive isolation - big fish like to mate with big fish; small fish with small fish In this case, preference genes don’t appear to be linked to size-determining genes; fish can just have the allele for “I find my own size to be sexy”, whatever that size is Thus, no gene flow between the two ecotypes of stickleback, although they are close relatives that diverged only a few thousand years ago in each lake Ecotype = different forms of one species that have not yet evolved full reproductive isolation (not species, yet) Parallel speciation in 3-spined sticklebacks