Unravelling the role of host plant expansion in the diversification of a Neotropical butterfly genus

Determining which traits and corresponding selective pressures initiate divergence
is key to understanding the causes of ecological speciation, and diversification in
phytophagous insects has often been thought to be driven by shifting and adapting
to new host plants 1]. Although the genus Melinaea is characterized by a recent and rapid diversification across much of the Neotropics
8]–11], we found that most species in this study co-occur with and utilize the same host
plant, J. parasitica, suggesting that diversification and speciation in this genus has mostly occurred
without changes in host plants. We did, however, find large differences in performance
on the novel host plant T. speciosa between the co-occurring M. mothone and the other species, consistent with local adaptation to host plant species.

But the fact that M. mothone has retained the ability to use and do equally well on both J. parasitica and T. speciosa, despite the fact that the former does not co-occur, and in addition to the absence
of oviposition preference for the co-occurring host species, suggests that the use
of a novel host plant is more likely due to niche expansion as a consequence of plasticity
for potential hosts. We also found a positive relationship between oviposition preference
and larval performance for the other Melinaea species, but the reduction in larval performance on the novel host plant Trianaea was not as pronounced as the decline in oviposition. Evidence for asymmetry between
oviposition preference and larval performance on novel hosts has been documented for
other herbivores, as a result of, for example, plant chemistry, competition or enemy-free
space, host abundance, larval conditioning during development 19]–21]. It has been postulated that oviposition on novel hosts that are suitable for larval
development, be it a result of oviposition mistakes or the result of a labile oviposition
strategy, might enable host range expansions 21]–23]. Shifts by herbivorous insects are sometimes restricted to related plant species,
but also occur on unrelated plants, and can be mediated by chemical similarities of
the new host, or can be explained by patterns of parallel cladogenesis, and/or increased
ecological opportunities (i.e., hosts that are geographically available) (see 24] and references therein). Our results suggest that some potential to oviposit, feed,
and survive on the related but novel host plant Trianaea is already present in the genus Melinaea, which is consistent with the use of multiple hosts by this group of butterflies
throughout their geographic range (see 11]).

Furthermore, a key prediction of ecological speciation is that traits that prevent
gene flow from eroding adaptation are likely those that evolved early, either directly
as the result of adaptive divergence, or as the result of selection preventing the
formation of maladaptive hybrids 25]–27]. In the genus Melinaea, McClure Elias 11] observed strong assortative mating among taxa, possibly as a result of homogamy for
colour pattern, even in very recently diverged lineages such as the M. marsaeus subspecies, and even in the absence of host plant differentiation. In this genus,
it is likely that plasticity in host use has enabled for a large geographical distribution,
which in turn likely exposed populations to a different suite of potential Müllerian
mimics. For example, Melinaea mothone has distinct elevational preferences and is associated with typically Andean mimicry
complexes, including another Melinaea species which shares the same colour pattern, M. isocomma. Because predation pressure differs for different mimetic communities 28], spatially segregated populations of Melinaea butterflies are likely selected to harbour different colour patterns that coincide
with those patterns that are most common within their given mimetic environment 29], 30].

Through the maintenance of a spatial mosaic of mimetic colour patterns, predation
on Müllerian mimics constrains geographical distribution and allows for different
species or subspecies, even those with similar ecological niches, to exist in different
regions 31]. Migrants between populations suffer reduced survival because they are non-mimetic
outside their habitat and suffer higher levels of predation attacks, which can directly
reduce gene flow between populations by lowering the rate of heterospecific encounters
32]. Switches in mimicry can also lead to pleiotropic changes in mate choice, as assortative
mating often coevolves with colour pattern, and reinforcement against maladaptive
non-mimetic hybrids 33], 34].

Over time, accumulated differences of other ecological aspects, including but not
limited to host plant use, will ultimately accumulate, leading to reproductive isolation
and speciation. Nevertheless, the expansion of the potential host plant repertoire,
rather than host shifts per se, may have been an important driver of diversification,
because more potential host plants means a larger area of distribution and, as such,
a larger number of potential niches 3], 4], 35].