Frequency-dependent hybridization contributes to habitat segregation in monkeyflowers

Spatial segregation of closely related species is usually attributed to
differences in stress tolerance and competitive ability. For both animals
and plants, reproductive interactions between close relatives can impose a
fitness cost that is more detrimental to the rarer species.
Frequency-dependent mating interactions may thus prevent the establishment
of immigrants within heterospecific populations, maintaining spatial
segregation of species. Despite strong spatial segregation in natural
populations, two sympatric California monkeyflowers (Mimulus nudatus and
M. guttatus) survive and reproduce in the other’s habitat when
transplanted reciprocally. We hypothesized that a frequency-dependent
mating disadvantage maintains spatial segregation of these monkeyflowers
during natural immigration. To evaluate this hypothesis, we performed two
field experiments. First, we experimentally added immigrants in varying
numbers to sites dominated by heterospecifics. Second, we reciprocally
transplanted arrays of varying resident and immigrant frequency. Immigrant
seed viability decreased with conspecific rarity for M. guttatus, but not
M. nudatus. We observed immigrant minority disadvantage for both species,
but driven by different factors– frequency-dependent hybridization for M.
guttatus, and competition for resources and/or pollinators for M. nudatus.
Overall, our results suggest a major role for reproductive interference in
spatial segregation that should be evaluated along with stress tolerance
and competitive ability.

近缘物种的空间隔离通常归因于胁迫耐受性与竞争能力的差异。无论是动物还是植物，近缘物种间的繁殖互作均可产生适合度代价，且该代价对稀有物种更为不利。因此，频率依赖型交配互作可阻止外来个体在异种种群中定殖，进而维持物种的空间隔离。尽管自然种群中存在显著的空间隔离，但两种同域分布的加州猴面花（*Mimulus nudatus*与*M. guttatus*）在相互异位移植后，均可在对方的生境中存活并繁殖。我们提出假说：在自然迁入过程中，频率依赖型交配劣势维持了这两种猴面花的空间隔离。为验证该假说，我们开展了两项野外实验：其一，以不同数量梯度向异种优势生境中接入外来个体；其二，以不同的本地种群与外来个体频率配比，构建相互异位移植实验阵列。研究发现，对于*M. guttatus*，外来个体的种子活力随其同种个体的稀有程度升高而降低，而*M. nudatus*则未表现出该规律。我们在两个物种中均观察到了外来个体的弱势效应，但二者的驱动机制各不相同：*M. guttatus*的弱势效应由频率依赖型杂交介导，而*M. nudatus*则由资源与（或）传粉者的竞争所驱动。综上，本研究结果表明，繁殖干扰在物种空间隔离中发挥着重要作用，该作用应与胁迫耐受性及竞争能力一同纳入评估范畴。